research articles on bioremediation of environmental pollution

• Open access
• Published: 13 August 2024

Microbial remediation of polluted environment by using recombinant E. coli : a review

• Samriti Sharma 1 ,
• Shruti Pathania 2 ,
• Suhani Bhagta 3 ,
• Neha Kaushal 2 ,
• Shivani Bhardwaj 4 ,
• Ravi Kant Bhatia 5 &
• Abhishek Walia 4  

Biotechnology for the Environment volume  1 , Article number:  8 ( 2024 ) Cite this article

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An increased amount of toxins has collected in the environment (air, water, and soil), and traditional methods for managing these pollutants have failed miserably. Advancement in modern remediation techniques could be one option to improve bioremediation and waste removal from the environment. The increased pollution in the environment prompted the development of genetically modified microorganisms (GEMs) for pollution abatement via bioremediation. The current microbial technique focuses on achieving successful bioremediation with engineered microorganisms. In the present study, recombination in E. coli will be introduced by either insertion or deletion to enhance the bioremediation properties of the microbe. Bioremediation of domestic and industrial waste performed using recombinant microbes is expensive but effectively removes all the waste from the environment. When compared to other physicochemical approaches, using microbial metabolic ability to degrade or remove environmental toxins is a cost-effective and safe option. These synthetic microorganisms are more effective than natural strains, having stronger degradative capacities and the ability to quickly adapt to varied contaminants as substrates or co-metabolites. This review highlights the recent developments in the use of recombinant E. coli in the biodegradation of a highly contaminated environment with synthetic chemicals, petroleum hydrocarbons, heavy metals, etc. It also highlights the mechanism of bioremediation in different pollution sources and the way in which this genetically altered microbe carries out its function. Additionally, addressed the benefits and drawbacks of genetically engineered microbes.

Introduction

The advent of global industrialization has brought about critical environmental challenges with pollution being a significant concern. While industrialization has contributed significantly to economic development, technological advancements, and improved living standards for human being, but simultaneously, it has also led to adverse environmental impacts particularly in the context of pollution of the environment [ 1 ]. Environmental pollution refers to the degradation of the natural environment because of the introduction of pollutants. There are several types of environmental pollution including air pollution, water pollution, and soil pollution [ 2 , 3 , 4 , 5 ]. Pollutants encompass substances that, while sometimes naturally occurring, are deemed contaminants when surpassing natural levels. Pollutants can be categorized into biodegradable and nonbiodegradable types. Biodegradable pollutants, like phosphates and organic waste, can be broken down by living organisms. In contrast, nonbiodegradable pollutants, such as plastics, metals, pesticides, glass, and radioactive isotopes, resist decomposition by living organisms, persisting in the ecosphere for extended periods [ 6 ].

Environmental pollution, a ubiquitous and pressing issue, casts a looming shadow over the planet, threatening the delicate balance of ecosystems and endangering the health of both flora and fauna, including humans. From air and water pollution to soil contamination, the consequences of human activities on the environment are manifold and far-reaching [ 7 ]. The call for India to prioritize environmental protection amid its rich biodiversity and stark socio-economic disparities has never been more urgent. Joutey et al. and Rabani et al. [ 8 , 9 ] underscore the critical need for India to balance economic development with environmental conservation. The government of India has taken major steps to prevent pollution in our country (Table  1 ). Addressing environmental pollution requires a combination of regulations, technological advancements, public awareness, and sustainable practices to minimize and mitigate the impact of pollutants on the planet. Numerous laws have been enacted to tackle the escalating pollution levels and set emission standards [ 10 ]. These legislative measures represent crucial milestones in India’s environmental stewardship journey.

Dealing with pollution is a complex challenge, and various methods, both physical and chemical, have been employed to address the pervasive environmental issues (Table  2 ). However, their effectiveness and cost often limit their widespread use. Natural solutions, while safe and effective, face challenges due to the rapid accumulation of pollution from industrialization and the presence of nonbiodegradable synthetic materials [ 11 , 12 ]. Physical methods, such as filtration and soil excavation, can be time-consuming and costly. Chemical alternatives, on the other hand, may pose inherent dangers to the environment and human health. Moving forward, it is imperative for India to adopt a holistic approach to environmental conservation—one that integrates environmental considerations into all aspects of policymaking and development planning. This approach should prioritize the protection of ecosystems, biodiversity, and public health while fostering sustainable economic growth and social equity. Advances in science and technology play a crucial role in pollution mitigation.

In response to these limitations, bioremediation has emerged as a promising and environmentally friendly approach. Bioremediation involves the use of microorganisms to assimilate, digest, or transform hazardous substances into less harmful or nontoxic forms [ 13 , 14 , 15 ]. Microorganisms exhibit remarkable capabilities in degrading, detoxifying, and even accumulating toxic organic and inorganic substances [ 16 , 17 ]. The use of genetically modified organisms (GMOs), such as the genetically modified Escherichia coli , has become a powerful tool in the field of bioremediation. These engineered microorganisms are designed to efficiently remove toxins that indigenous bacteria may struggle to break down, offering a targeted and effective approach to environmental cleanup [ 18 ]. In contemporary bioremediation methods, genetically modified organisms play a pivotal role in addressing environmental pollution, particularly in situations where natural bacterial populations are insufficient to handle specific pollutants. The introduction of a foreign gene into bacteria transforms them into unique strains with enhanced capabilities for rapidly breaking down pollutants, such as hydrocarbons, in the environment [ 19 ]. The use of genetically modified E. coli in bioremediation has several advantages such as precision, efficiency, and versatility. However, it is essential to consider potential ethical and ecological concerns associated with the release of genetically modified organisms into the environment. Robust containment measures and thorough risk assessments are crucial to prevent unintended consequences. Therefore, in this article, the use of genetically modified E. coli in bioremediation is discussed which exemplifies the intersection of biotechnology and environmental science, offering innovative solutions to address pollution challenges. As technology continues to advance, the application of genetic engineering in bioremediation holds significant promise for developing tailored and efficient approaches to environmental cleanup.

• Bioremediation

To deal with pollution, a variety of methods (physical and chemical) are available. Due to their high cost and low effectiveness, most of them are of limited use. Physical methods are time-consuming and expensive, whereas chemical alternatives are inherently dangerous. Natural solutions are safe and effective, although they are sluggish and becoming less effective as a result of industrialization’s rapid pollution buildup and nonbiodegradable synthetic materials [ 11 , 12 ]. Bioremediation is gradually becoming the standard method for restoring contaminated with heavy metals because it is efficient and cost-effective technology for the transformation of contaminants [ 13 , 14 , 15 ]. Biodegradation is a series of chemical reactions that occur in the presence of living organisms such as bacteria, fungi, yeast, algae, and insects in an environment with optimal light, temperature, and oxygen [ 20 ]. Microbes mitigate heavy metals and improve soil fertility, and plant development makes them more preferable source for bioremediation. The molecular nature, gene and enzyme induction, metabolite production, growth efficiency, and survival rate all influence individual bacteria’ potential to act as bioremediation agents [ 21 ]. At higher moisture rate, anaerobic condition persists which slow down the degradation rate. In cold condition, microbial degradation of heavy metal is slow, as metabolic activities are inhibited as the microbial transport routes are frozen by the sub-zero water [ 22 , 23 ]. Similarly, at higher temperature, the rate of heavy metal solubility increases, which increases their availability and the rate of microbial biodegradation [ 24 ]. The rate of microbial biodegradation is determined by the metal or pollutant’s chemical structure, bioavailability, concentration, toxicity, and stability. The degradation of the n-alkanes is more effortless in comparison to the branched alkanes, aromatics with low molecular weight, hydrocarbons with high molecular weight, and the asphaltenes [ 25 ]. Molecular mechanisms play a crucial role in deciphering the microbial metabolism, genes, characteristics, variety, and fluctuations of microorganisms engaged in microbial remediation. Metabolic and protein analysis, sequencing, and the utilization of sophisticated bioinformatics tools are specifically employed to decipher the various categories of microorganisms and the factors influencing them in the bioremediation process [ 23 ].

Microorganisms currently employed in bioremediation have the potential to be genetically engineered in order to augment their enzymatic production, thereby amplifying their capacity for biodegradation. These organisms’ genetic architecture makes them useful for biodegradation, biotransformation, biosorption, and bioaccumulation [ 26 ] (Fig.  1 ). The use of recombinant DNA allows an organism to develop the ability to digest a xenobiotic via degradative genes. Recombinant microorganisms and genetically modified microbes have been used as an effective technique for pollution breakdown [ 27 ]. In the current bioremediation technique, genetically modified organisms are employed to efficiently eliminate pollutants that native bacteria are unable to decompose [ 18 ]. There are varieties of bacteria reported to be capable of feeding on hydrocarbons under anaerobic and aerobic conditions [ 28 ]. Toxic substances may be converted to nontoxic ones by the bioremediation process by a variety of bacteria species such as Achromobacter , Pseudomonas , Dehalococcoides , Rhodococcus , Comamonas , Burkholderia , Alcaligenes , Bacillus subtilis , Aspergillus niger , Deinococcus radioduran , Acidithiobacillus ferrooxidans , Mesorhizobium huakuii , Pseudomonas K-62, Ralstonia , Rhodopseudomonas palustris , and Sphingomonas [ 29 ]. Similarly, nitrate-reducing bacterial strains, Brevibacillus sp. and Pseudomonas sp., were identified in petroleum-contaminated soil. Bacillus , Corynebacterium , Staphylococcus , Streptococcus , Shigella , Alcaligenes , Acinetobacter , Escherichia , Klebsiella , and Enterobacter were the best hydrocarbon-degrading bacteria [ 30 ].

Different approaches adapted by the microbes for the degradation of toxic compounds

Microbe’s genetic sequences have been manipulated keeping specific goal in mind [ 31 ]. The term “genetically engineered organisms” (GEMs) refers to microorganisms (bacteria, fungi, and yeast, among others) that have been altered by humans utilizing molecular biology in vitro procedures [ 32 ]. There has been an explosion in the expansion of genetic engineering and recombinant DNA in breeding microorganisms, resulting in a huge number of bacteria with effective engineering that boosted pollutant-degrading abilities [ 18 , 27 , 33 ]. Bioremediation research is awaiting the introduction of gene editing technologies that produce knock-in and knockout. According to recent articles, researchers have mostly used the CRISPR-Cas system with model organisms such as Pseudomonas or E. coli [ 34 ]. Even non-model organisms like Achromobacter sp. HZ01 and Comamonas testosteroni may be employed for bioremediation due to new insights into CRISPR tools and the synthesis of gRNA to express function-specific genes pertinent to remediation [ 35 , 36 ]. In experiments involving organophosphate and pyrethroid bioremediation, genetically altered Pseudomonas putida KT2440 was employed [ 37 ]. White rot fungus produces enzymes that break down polycyclic aromatic hydrocarbons (PAHs), TNT (2,4,6-trinitrotoluene), and polycyclic aromatic hydrocarbons (PCBs). When the enzyme esterase D combines with the insecticide endosulfan (an organochlorine), it produces simpler molecules. LiP-encoded hemoproteins in Phanerochaete chrysosporium degrade PAHs [ 38 ].

Recombinant E. coli in bioremediation

E. coli is a rod-shaped facultative coliform bacterium belonging to the genus Escherichia that measures only about 1 µm long by 0.35 µm wide. It is one of the model organisms used in bioremediation (Fig.  2 ). E. coli is generally known as the “work horse” of molecular biology for its fast growth rate in chemically defined media and the various tools available for its genetic modifications. E. coli harbors a genome with features like an organized structure, a remnant of many phages, insertion sequences (IS), and high transport capacity towards the cytoplasm [ 39 ]. E. coli is a preferred host for gene cloning due to the ease with which DNA molecules may be introduced into the cells. Protein production in E. coli is expected due to the strain’s rapid growth and high protein expression levels [ 40 ]. Various studies show that enteric bacterium like E. coli form phenol and p-cresol when grown on natural media (peptone and casein media) as well as in chemically defined media, i.e., L-tyrosine and p-hydroxybenzoic acid media [ 41 ]. According to a study conducted by Burlingame and Chapman [ 42 ] in 1983, it was found that E. coli has the capability to mineralize several aromatic acids, such as PA (phenylacetic acid), HPA (hydroxyphenylacetic acid), PP (phenyl propionic acid), 3HPP (hydroxyl phenyl propionic acid), and 3HCl. These research findings emphasized the ability of E. coli to break down and utilize a diverse range of aromatic acids [ 22 ]. An E. coli bacterium that has been genetically modified is employed as a highly effective agent in the process of bioremediation. The incorporation of a gene into bacteria results in the conversion of the bacteria into a distinct strain that possesses the ability to efficiently eliminate hydrocarbon pollutants from the surrounding environment (Fig.  3 ) [ 19 ]. There exist multiple methods for manipulating microbial genetics through genome editing, each of which is quite efficient and has been used in E. coli genome editing, making it capable of degrading pollutants and converting them to less harmful molecules [ 43 ]. The curli of an E. coli cell was genetically modified to produce BIND-PETase [ 40 ]. The E. coli SE5000 strain underwent genetic modification by introducing the nixA gene, which enables the expression of a nickel transporting system. This system has the ability to degrade nickel from aqueous system [ 44 , 45 ]. The E. coli FACU strain possesses a significant capacity to reduce Cr (IV) to Cr (III) exhibiting great potential as a viable agent in the bioremediation of hazardous chromium species in aerobic environmental conditions [ 46 ].

Mechanism of biosorption on the basis of cell metabolism and its location within cell or metal removable

Overview of bioremediation methods

General mechanism of degradation of pollutant by recombinant microbe

Genetic manipulation possesses the ability to create or mend microorganisms, leading to the development of biological detection systems that exhibit enhanced internal robustness, specificity, and resilience in various environments. Genetically engineered microorganisms (GEM) refer to microorganisms that have undergone genetic modifications using techniques of genetic engineering (inspired by the natural genetic exchange observed between microorganisms) [ 47 , 48 ]. GEMs (genetically engineered microbes) have shown promise in the bioremediation of soil, groundwater, and activated sludge, with improved degrading capabilities for a variety of chemical contaminants [ 28 ]. Microbes possess inherent biological mechanisms that enable them to withstand intense metal stress or eradicate metals from their surroundings. Microbial bioremediation employs the following mechanisms [ 49 ]:

(1) Cell wall components or intracellular metal-binding proteins and peptides, such as metallothioneins (MT) and phytochelatins, play a crucial role in sequestering toxic metals. Additionally, substances like bacterial siderophores, which are mainly catecholates, are also involved in this process. It is worth noting that fungi produce hydroxamate siderophores [ 50 ].

(2) Altering metabolic processes directly blocks metal uptake.

(3) Enzymes are used to convert metals into harmless forms.

(4) Efflux mechanisms have the potential to decrease metal levels within the intracellular milieu.

Environmental contaminants such as chlorobenzene acids, toluene, and other halogenated insecticides and toxic wastes are broken down into less harmful forms by using important genes. A different plasmid is required for each chemical [ 51 , 52 ]. Plasmids are classified into four groups [ 53 ].

1) OCT plasmid (degrades octane, hexane, and decane).

2) XYL plasmid (degrades xylene and toluenes).

3) CAM plasmid (degrades camphor).

4) NAH plasmid (degrades naphthalene).

The appearance and dissemination of genes that break down pesticides can yield a beneficial impact on the elimination of hazardous waste from the surroundings. The potency of E. coli in the degradation of various pollutants has been shown in Table  3 . The genetically engineered strain of E. coli is able to express the Hg 2+ and metallothionein transport systems. Excessive exposure to Saccharomyces cerevisiae glutathione S-transferase fusion protein and pea metallothionein significantly increased Hg 2+ expression delivered by MerP and MerT, which protect cells from Hg 2+ [ 54 , 55 ]. Similarly, horizontal gene transfer (HGT) methods have been employed for incorporating petrol-contaminated organisms with E. coli carrying the vector pSF-OXB15-p450 cam fusion, which showed that E. coli bacteria are useful for the degradation of heavy metals [ 56 ]. Recombinant E. coli that expresses the metallothionein gene ( Neurospora crassa ) for Cd uptake was created using plasmid-encoded biochemical information and genetic engineering techniques, yielding a significantly faster Cd uptake than the donor microbe [ 57 ].

Different types of pollution and their bioremediation using recombinant E. coli

Soil contamination.

Soil is an essential ecosystem consisting of both living and nonliving elements. The entirety of the natural world relies on soil in various ways. It serves as a connection between the biosphere, atmosphere, and hydrosphere, thereby playing a crucial role in maintaining the ecological equilibrium [ 67 ]. There exists a disagreement in the definition of “soil contamination.” According to certain viewpoints, soil is deemed contaminated when the concentration of chemicals exceeds its typical range. While some individuals express concerns regarding the establishment of the standard range for pollutants. Hence, it can be asserted that “soil which is unsuitable for utilization and incapable of fulfilling its purpose is deemed as contaminated” [ 68 ]. The quality of soil and its role in ecological balance are affected by the addition of soil contaminants due to natural processes and human activities like industrial wastes, the use of fertilizers in agricultural activities, and domestic and commercial construction [ 69 ]. Broadly, two types of contaminants contribute to soil pollution: inorganic and organic. In the category of inorganic pollutants, heavy metals are placed at the top of the list and are present in most of the contaminated sites. The most common toxic heavy metal contaminants found in soil include mercury (Hg), arsenic (As), copper (Cu), cadmium (Cd), chromium (Cr), Zinc (Zn), lead (Pb), and nickel (Ni) [ 70 ]. These soil contaminants sink into the soil through bad agricultural practices, inefficient industrial effluent disposal techniques, unauthorized waste dumping, etc. The persistence of heavy metals in natural environments presents a more formidable obstacle in comparison to organic contaminants, as they exhibit resistance to both microbial and chemical degradation. As a result, the elimination of heavy metals becomes a long-lasting challenge once they are introduced [ 71 ]. Organic contaminants encompass carbon-containing substances, regardless of the presence or absence of functional groups within their structures. The list of organic contaminants that contribute to soil pollution includes insecticides (e.g., captan, benomyl, endosulfan, heptachlor), herbicides (atrazine, alachlor, acetochlor, etc.), oil hydrocarbons (e.g., alkanes, alkenes), chlorinated compounds (e.g., polychlorinated biphenyls (PCB), polychlorinated dibenzodioxins (PCDD), polychlorinated dibenzofurans (PCDF)), aromatic hydrocarbons (e.g., BTEX, i.e., benzene, toluene, ethylbenzene, xylene), biocides (benzalkonium chloride), and polycyclic dibenzo-p-dioxins (e.g., benzopyrene, chrysene, fluoranthene) [ 72 ]. Persistent organic pollutants (POPs) are classified as organic contaminants, which are regarded as the most prioritized category of organic contaminants due to their high toxicity, carcinogenic properties, and ability to bioaccumulate in the environment [ 73 ]. Taking this into consideration, numerous nations have implemented limitations or outright prohibited the utilization and production of persistent organic pollutants (POPs). The POP compounds encompass substances such as DDT, endrin, hexachlorobenzene, PCBs, PCDD, PCDF, and others [ 68 , 74 ] (Fig.  4 ).

Direct enzymatic and indirect mobilization of radionuclides by metal-reducing microorganisms via capturing of electrons derived by organic compounds (lactate and acetate)

Traditionally, various techniques are used to remove the soil contaminants, including extraction and separation techniques, thermal methods, chemical methods, microbial treatment methods, solid waste treatments, and phytoremediation (Table  4 ). The existing treatments for soil pollution, as discussed above, are not very successful in the removal of contaminants; sometimes, they bring down the concentration of contaminants at the cost of soil quality. Some of the techniques are also less cost-effective [ 75 , 76 ]. The main objective of soil remediation is not just the elimination of contaminants but also to restore the quality of the soil. So, we need to shift towards a new approach that gives better and more desirable results in terms of the elimination of pollutants and the restoration of soil quality [ 77 ]. Bioremediation is one of those approaches on which we can rely. In recent years, bioremediation has emerged as a great alternative to existing treatments as it is economical and does not compromise the health of the soil [ 78 ].

Recombinant E. coli strain used for bioremediation of soil

The various studies done by Almaguer-Cantú et al. [ 80 ] on the removal of heavy metal contaminants from soil reported that genetically modified E. coli cells with overexpression of pea metallothionein MT improve the biosorption of Ni 2+ and efficiently remove Ni 2+ contamination from the affected sites. The elimination of hazardous metals from a polluted area through the utilization of biosorbent cell surface components of microorganisms is known as biosorption [ 81 ]. These biosorbent cell surface moieties are present on the outer surfaces of fungi, algae, and bacteria. Bacteria are widely regarded as the superior biosorbent when compared to other microorganisms [ 82 ]. This is primarily attributed to their possession of chemosorption sites such as teichoic acid, as well as their remarkable surface-to-volume ratio. These characteristics greatly enhance their biosorption capabilities [ 83 ]. In a study done in the United States for the removal of atrazine contamination from the contaminated fields by using recombinant E. coli encapsulating AtzA, which is responsible for the degradation of atrazine, they observed that after 8 weeks of inoculation, atrazine levels decreased by 52% and 77% (Table  5 ) in plots containing killed recombinant E. coli cells and combinations of phosphate, respectively [ 63 , 84 ].

The successful elimination of oil contaminants in soil caused by oil spills can be achieved through the introduction of genetically modified E. coli cells containing catabolic genes [ 92 ]. The overexpression of three enzymes, namely almA, xylE, and p450cam, results in the degradation of petroleum hydrocarbon. According to their research, this genetically modified E. coli was able to decrease the level of petroleum hydrocarbon concentration by as much as 46% after a period of 60 days following inoculation [ 56 ]. Mercury (Hg) is a hazardous heavy metal and a significant inorganic pollutant found in soil, which can have harmful consequences on the organisms inhabiting contaminated areas. When it infiltrates the human body through the food chain, it gives rise to serious ailments such as neural disorders and respiratory disorders, occasionally leading to fatality. Genetically modified E. coli JM109 cells can assist in eliminating the Hg 2+ contamination present in the soil [ 93 ]. This strain of E. coli has been genetically modified to produce the merT-merP protein and metallothionein, which are responsible for the accumulation of Hg 2+ in the organism [ 64 ]. E. coli SE5000, a genetically modified strain, possesses the GSM-MT and nixA genes. The nixA gene is accountable for the activation of the Ni 2+ transport system, enabling it to effectively eliminate Ni 2+ contamination. On the other hand, GSM-MT is responsible for the increased production of metallothionein in the form of a glutathione S-transferase fusion protein [ 94 ].

Air pollution

Despite the remarkable advancements in technology, society, and the provision of various services, the Industrial Revolution had a detrimental impact on human health due to the significant release of pollutants into the air ( http://www.who.int/airpollution/en/ ). Air pollution is the term used to describe the existence of detrimental substances in the atmosphere of our planet, which has adverse effects on both human well-being and the environment [ 95 , 96 ]. The increase in economic growth has been accomplished by elevated energy consumption. The rapid urbanization in India, coupled with swift economic progress, has led to a surge in air pollution levels within megacities [ 97 ]. Particulates, greenhouse gases, and smog-forming substances such as sulfur dioxide (SO 2 ), ground-level ozone (O 3 ), nitrogen oxides (NO 2 ), and volatile organic compounds, are all major air pollutants (VOCs) [ 98 , 99 ]. Air pollution has adverse effects not only on humans but also on the marine environment and is responsible for climate change too. The degradation of the earth’s atmosphere is closely linked to the relationship between climate change and air pollution. The elevated concentrations of methane, black carbon, aerosols, and tropospheric ozone disturb the incoming solar radiation. Consequently, the temperature is on the rise, leading to the melting of icebergs, ice, and glaciers [ 22 , 100 ]. The World Health Organization provides information on different categories of air pollutants, such as particle pollution, ground-level ozone, carbon monoxide, sulfur oxides, nitrogen oxides, and lead. In 2011, Delhi recorded a PM10 level of 198 μg m −3 , which exceeds the minimum limit by a factor of 10 [ 101 , 102 ]. In May 2014, the city of New Delhi earned the unfortunate distinction of being the most polluted city in the world, according to the World Health Organization (WHO). This was primarily attributed to the high concentration of particle matter (PM) with a diameter less than 2.5 µm, which exceeded 350 µg per cubic meter of air in New Delhi. ( http://www.theguardian.com/news/datablog/2015/jun/24/air-pollution-delhi-is-dirty-but-how-do-other-cities-fare ) [ 95 ]. A conference titled “Impact of Disease: Air Pollution as a Leading Cause” was organized in New Delhi on February 13, 2013, by the Centre for Science and Environment (CSE) in collaboration with the Health Effects Institute, Boston, USA, and the Indian Council of Medical Research, New Delhi ( http://www.cseindia.org/content/workshop-global-burden-disease-air-pollution-amongst-top-killers-india ).

Air pollution can be easily dispersed and transported between different areas. This detrimental pollution leads to significant issues for both the environment and human health. Consequently, it is imperative to discover effective decontamination strategies in order to cleanse the environment. The process of decontamination must be carried out in a manner that safeguards the well-being of both animals and humans while also promoting the circulation of clean air [ 31 ] (Perera and Hemamali, 2022). Consequently, there is an increasing desire to discover efficient methods for remediating polluted areas, whether partially or entirely, in order to restore their environmental integrity [ 103 , 104 ].

Degradation of air pollutant by recombinant E. coli microbe

Bacteria facilitate the breakdown of dangerous chemicals through an assimilative mechanism, wherein they acquire carbon and energy to support their growth, ultimately leading to the conversion of the compound into minerals [ 105 , 106 ]. The bacteria responsible for PAH degradation include Achromobacter sp . , Bacillus sp., Mycobacterium sp . , Burkholderia sp., Pseudomonas sp., Rhodococcus sp., Stenotrophomonas maltophilia , Sphingomonas sp., Xanthomonas sp., and Xanthomonas sp. [ 107 , 108 ]. The initial stage of hydrocarbon degradation involves the transformation of polycyclic aromatic hydrocarbon (PAH) or alkane chain into basic alcohol, subsequently converting into aldehyde and ultimately resulting in water, carbon dioxide, and biomass through oxidation. Oxidation also leads to the conversion of reduced sulfur molecules like H 2 S into inorganic sulfur and thiosulfate, forming corrosive sulfuric compounds [ 101 , 109 ]. H 2 S advance oxidation is completed by chemolithotrophs. Sulfate is ingested through the sulfate start pathway, which is made up of three responses: adenosine 5′-phosphorylation of APS, GTP hydrolysis, and APS 3′-phosphorylation to deliver 3′-phosphoadenosine 5′-phosphosulfate (PAPS) [ 110 , 111 ]. Microbes that degrade sulfate have the ability to use hydrocarbons and hydrolyze complicated chemicals in soil, according to Rennenberg [ 112 ]. Besides, a designed strain able of debasing PAHs was made in E. coli by communicating salicylate oxygenase, a protein encoded by bphA2cA1c from Sphingomonas yanoikuyae B1 [ 113 ]. The pGEX-AZR/ E. coli JM-109 strain was genetically engineered, resulting in enhanced efficiency for decomposing various azo dyes [ 114 ].

Water pollution

The express “water contamination” is characterized in an assortment of ways by different committees, with the objective of making strides the quality of our environment. Agreeing to the head of the science committee, Washington, USA, in 1965, characterized water contamination as an alteration within the physical, compound, and organic qualities of water that will cause risky impacts on human and maritime life. Nowadays, it is not only concerned with public health but also with destroying natural beauty, resources, aesthetics, and the conservation of water [ 115 , 116 ]. Numerous anthropogenic exercises are related to water contamination and have driven to water quality disintegration, like industrialization, chemical-related cultivating, broad urbanization, and populace development [ 117 ]. There are two sorts of sources that are included in water contamination, i.e., point sources and nonpoint sources. The coordinate identifiable source, or where coordinate association is appeared, is known as a point source, such as mechanical effluents, oil spills, and metropolitan and mechanical squander water effluents. In terms of nonpoint sources, diverse sources are included within the event of water contamination, primarily urban squander, runoff from rural areas, radioactive water (from atomic reprocessing plants), and contaminants that enter ground-level water [ 49 ]. Water contamination is caused by a variety of factors, the most prominent of which being urbanization (higher phosphorus concentrations in urban catchments sewage waste (massive increase in the growth of algae or plankton that facilitate huge areas of oceans, lakes, or rivers), industrial waste (wastes containing acids, alkalis, dyes, and other chemicals), agro-chemical waste (include fertilizers, pesticides which may be herbicides and insecticides), nutrient enrichment, thermal pollution (nuclear power and electric power plants, petroleum refineries, steel melting factories, coal fire power plant, boiler from industries), oil spillage (petrol, diesel, and their derivatives pollute seawater), acid rain pollution, and radioactive pollution (radioactive sediment, waters used in nuclear atomic plants, radioactive minerals exploitation, nuclear power plants) [ 65 , 118 , 119 ].

Water contamination is treated using a variety of physical and chemical approaches [ 75 , 94 ]. Screening (radioactive sediment, waters used in nuclear atomic plants, radioactive mineral exploitation, nuclear power plants), grit chamber (remove sand and egg shells), floatation (oils, fats, grease, sediment solids), and sedimentation tank clarifier are examples of physical treatments (remove heavier sludge solids), whereas chemical treatments are as follows: neutralization (it adjusts pH for maintaining acidity of water), flocculation, coagulation (solid removal, water clarification, lime softening by chemical flocculants and coagulants), oxidation (may reduce toxicity using biochemical oxygen demand), ozonation (degradation of organic and inorganic pollutants), and chlorination [ 115 , 120 ].

Drawbacks of physical and chemical methods

So many by-products are formed, chemical consumption is so high, physicochemical monitoring of effluents, capital and energy costs are so high, high sludge production and management of disposable, and techniques are expensive and toxic to the environment (Table  6 ).

Biological method used for water treatment

The biological method is the most common sanitizing method used for wastewater treatment, and it is also called secondary treatment, which involves the removal of organic matter from wastewater using bacteria and other microorganisms [ 137 ]. Wastewater typically contains pathogenic organisms, heavy metals, toxins, and organic matter (garbage, waste, and partially digested foods) [ 138 ]. Biological methods can be classified into two categories: (i) aerobic—takes place in the presence of oxygen and (ii) anaerobic—takes place in the absence of oxygen. Aerobic biological treatment involves many processes, i.e., the activated sludge process, trickling filters, aerated lagoons, and oxidation ponds. Due to its ease of use, rapidity, and efficiency, this process removes up to 98% of organic contaminants. Anaerobic biological treatment is used to treat high-strength wastewater (sludge degradation and stabilization). The process is slow as compared to aerobic; biogas production is one example of biodegradation of material where it overall converts up to 60% of organic solid mass ( http://neoakruthi.com/blog/biological-treatment-of-wastewater.html ) [ 139 ].

Some of the examples of microorganisms that are involved in the treatment of wastewater using different processes are gram-negative bacteria (proteobacteria) for the elimination of organic elements and nutrients, Bacillus , Bacteroidetes, Acidobacteria, Chloroflexi, Tetrasphaera , Trichococcus , Rhodobacter , Pseudomonas , E. coli , Hyphomicrobium ascomycetes fungi, Nitrosomonas , etc. [ 137 , 138 , 140 , 141 ]. For specific contaminant degradation, predominantly well-defined microorganisms are used.

To improve the potency of proteins to overexpress the desired character for degradation by transforming microbes using genetic engineering approaches where they are transfected with genes that encode catabolic enzymes. Nowadays, genetically engineered microorganisms (GEM) are the most feasible xenobiotic-degrading microorganisms ( E. coli and Pseudomonas putida ) in wastewater treatment, and with the help of GEM, we can improve the bioaugmentation process. These GEMs have been used to degrade hexane, oil spills, xylene, toluene, camphor, trichloroethylene, etc. because of their high degradative capacities for various pollutants in wastewater [ 131 , 142 ]. Manipulation of the oil-degrading Pseudomonas bacterium with plasmids containing genes encoding catabolic enzymes used in the degradation of aromatic compounds [ 143 , 144 ]. For biodegradation of atrazine, metal removal, and direct blue dye in waste water, a genetically modified E. coli strain has been used [ 145 , 146 ].

Genetically modified E. coli involved in wastewater treatment

Mercury (Hg) is the most dangerous heavy metal that can be released into the environment through industrial wastewater. Mercury can be removed from contaminated water, soil, or sediment by the GE E. coli strain JM109 [ 43 ]. Mercury can be removed from a contaminated site using GE bacteria that possess the MerA gene [ 147 , 148 ]. GE E. coli has been discovered to digest trichloroethylene after being transformed with a variety of phenol catabolic genes such as pheA, pheB, pheC, pheD, and pheR. Nickel (Ni) is perhaps the most tenacious toxin, and it can be extracted from water by the GE E. coli SE5000 strain [ 149 ]. In this way, GE microorganisms can help with the bioremediation of heavy metals from degraded sites.

Safety of using recombinant E. coli strain for treatment of pollutants

Artificial generation of pollutants takes place by various by-products produced by the modern human world, which leads to toxicological impacts on nature. With growing awareness about the direct and indirect impacts of environmental pollution on ecosystems, efficient, cost-effective, and environmentally safe methods are being developed for the treatment of pollutants. The rapid rise in the rate of industrialization and the manufacturing of harmful toxic products leads to a change in the homeostatic balance of ecological biodiversity. Recombinant DNA technology emerged in 1972 and became the cutting-edge technology in the modern world, leading to the mass production of human insulin, human growth hormones, interferon, and the hepatitis vaccine [ 150 ]. In medical sciences, delivery made by this technology has set mild stones to combat pollution. For this purpose, genetically modified organisms (GMO) produced by recombinant DNA technology are used as a promising option for the treatment of pollutants, and many reports have also been published in this context [ 151 , 152 ]. There are a variety of pollutants that are increasing at an alarming rate in the environment and need to be monitored.

The common pollutants that are to be taken into consideration are heavy metals, high density petroleum hydrocarbons (mercury, lead, arsenic, cadmium, etc.), polymers, chlorinated hydrocarbons, pesticides, insecticides (polycarbonates, polyethylene, polyurethane, polypropylene, etc.), explosives, detergents (GTN, TNT, and RDX), etc. [ 153 , 154 ]. The combination of biotechnology and recombinant DNA technology is improving pollutant-degrading microbes through genetic modifications and strain improvement of specific metabolic and regulatory genes that are crucial in biodegradation [ 30 ]. Chakrabarty [ 155 ] established the bar by patenting petroleum oil pollution bioremediation, which was the first step towards using recombinant DNA technology for pollution mitigation. The most important and prominent tools for recombinant DNA technology are GMOs, which aid in the bioremediation of pollutants. Although they are potential deliverables, they need statutory clearance to be used in an open environment in many countries. So various regulatory guidelines are framed in different countries for their safe use.

The recombinant E. coli K-12 strain is extensively used for pollution control as it does not colonize the human gut and is non-pathogenic [ 156 ]. Further, it has a simple expression system as compared to other higher-level organisms and a large quantity of well-characterized genomic databases. Although certain scientific considerations are to be taken into account while assessing the environmental use of this recombinant microorganism by selecting appropriate safety measures, this may pose some negative impact on the environment [ 157 ]. The bioremediation process is monitored indirectly by measuring the polluted site’s redox potential as well as temperature, pH, electron acceptor and donor concentrations, oxygen content, and concentrations of breakdown products (e.g., carbon dioxide), and petroleum-contaminated environments are analyzed by bacterial biosensors [ 158 , 159 ]. In addition, microbial biosensors are increasingly being used to detect contaminants in systems based on reporter genes.

The specific metals in cellular environments are responsible for the expression of resistance genes, and this specificity of tight regulation is exploited in such biosensors [ 154 ]. The promoters and regulatory genes present in resistance operons are being used to construct metal-specific biosensors (promoter-reporter gene fusions) [ 160 ]. In addition to chemical analysis, metal-specific biosensors can be used:

To regulate pollutant concentration

Bioavailable metal concentration in the samples [ 110 ]

Thus, currently existing risk assessment and safety methods are being used to characterize the consequences of human exposure to such E. coli strains. Further, key difficulty lies in the assessment of interactions of the microorganism with the existing ecosystem. For example, an introduced E. coli strain may pass genetic material to other microbes, altering the environment and resulting in secondary impacts. Thus, two important areas of investigation related to establishment and proliferation are as follows:

(i) Fate of the recombinant E. coli strain and environmental transfer.

(ii) Interaction with the ecosystem.

This knowledge of recombinant E. coli transport and its fate (or survival) is useful for assessing potential exposures of nontarget organisms or nontarget areas and rendering it safe for remediation of pollutants [ 161 , 162 ].

Policy regarding regulation of genetically modified microorganisms

The recent advancements in genetic manipulation offer vast potential and are being utilized in various innovative experiments and applications. These progressions have raised apprehensions among researchers in the biological sciences and other related fields regarding the safe conduct of research in this domain. Genetically modified organisms (GMOs) and their products are regulated in India under the “Rules for the manufacture, use, import, export & storage of hazardous microorganisms, genetically engineered organisms or cells, 1989” (referred to as Rules, 1989) notified under the Environment (Protection) Act, 1986 [ 163 ]. The Ministry of Environment, Forest, and Climate Change, the Department of Biotechnology, and state governments enforce these rules through six competent authorities. Six competent authorities and their composition have been notified under these rules that include the following: rDNA Advisory Committee (RDAC), Institutional Biosafety Committee (IBSC), Review Committee on Genetic Manipulation (RCGM), Genetic Engineering Appraisal Committee (GEAC), State Biotechnology Coordination committee (SBCC), and District Level Committee (DLC). The Recombinant DNA Advisory Committee (RDAC) has been established by the department for this specific reason. A publication outlining the Recombinant DNA Safety Guidelines has been released, based on the latest scientific knowledge, to regulate the use of this technique in research, production, and various applications. In 2014, the Department of Biotechnology (DBT) established a specialized task force focused on “Genome Engineering Technologies and their Applications.”

The Coordinated Framework for Regulation of Biotechnology was issued in 1986 by the Office of Science and Technology Policy (OSTP) in United States of America (USA). The framework detailed the allocation of regulatory duties among the many authorities that deal with pesticide, food, and agricultural goods. Therefore, in compliance with the framework, the US Environmental Protection Agency (US EPA) regulates microorganisms and other genetically engineered constructs intended for pesticidal purposes and subject to the Federal Insecticide Fungicide and Rodenticide Act (FIFRA) and the Federal Food Drug and Cosmetic Act (FFDCA); USDA APHIS regulates microbes that are plant pests under the Plant Protection Act (PPA) and the National Environmental Policy Act (NEPA). Additionally, certain genetically modified microbes employed as biofertilizers, bioremediation agents, and to produce other industrial compounds including biofuels under the Toxic Substances Control Act (TSCA) are regulated by the US EPA (EPA 1999) [ 164 ].

The European Union (EU) has put in place a number of legal tools to guarantee the safety of goods made with or containing GMMs. A product must undergo a scientific risk assessment before it is allowed to be sold. A guidebook for the risk evaluation of genetically modified organisms (GMOs) in food or feed products has been released by the European Food Safety Authority’s (EFSA) GMO Panel (EFSA, 2011) [ 165 ]. The evaluation is divided into two sections: the GMOs characterization and any potential impact the modification may have on the product’s overall safety.

Genetic engineering methods have provided enough opportunities to remove pollutants and toxins from the environment. Comparing this technology with conventional technologies, it is less expensive and more ecologically friendly. It is important to consider environmental factors that may influence the bioremediation of contaminated sites. Microorganisms have an optimal environment for maximum performance as well as a limit of adaptation to certain environmental conditions. A range of biochemical, microbiological, ecological, and genetic factors influence the rate of bioprocessing and biodegradation of contaminants by genetically engineered bacteria for environmental cleanup. Scientists are continually uncovering new unique genes that can be used to generate new constructs and eventually a new strain that aids in the manufacture of derivative routes for new synthetic compounds, as well as the introduction of biodegradation capabilities in a variety of locations. Even with their great potential and encouraging results in the treatment of pollutants by recombinant host bacteria, recombinant bacteria still face a number of difficulties in the process of treating pollutants. In a complex environment with several substrates and numerous microbial interactions, only a small number of modified bacteria are involved in the treatment and removal of toxins. The greatest way to increase biodegradation variety is to use a plasmid with multiple operons rather than multi-plasmids with favorable qualities as plasmids are not only compatible but also incompatible. Protoplast fusion technique has demonstrated promising outcomes in the breeding of biodegradation-engineered bacteria, in addition to plasmids, which is a good thing. Recombinant bacterial strains were produced using the protoplast fusion process; however, the strains also contained genes that were unnecessary or harmful to breakdown. It is also important to follow the correct regulatory procedures for the safe containment and use of GMOs in bioremediation processes.

The subsequent stages of bioremediation research involve discovering and comparing gene and protein sequences that are efficient at eliminating contaminants, even though genomics, metabolomics, and proteomics in bioremediation help explore potential solutions to particular pollutants. GMOs have the ability to clean up a variety of contaminated soil and waste effluents. Utilizing bioremediation in tandem with other physical and chemical techniques can offer an all-encompassing strategy for eliminating pollutants from the surroundings and has the potential to overcome current challenges. It seems to be a long-term treatment; thus, more study in this field is required.

Availability of data and materials

No datasets were generated or analysed during the current study.

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I acknowledge the Department of Microbiology, CSK Himachal Pradesh Agricultural University, Palampur, for providing necessary funding to carry out this work.

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Sharma, S., Pathania, S., Bhagta, S. et al. Microbial remediation of polluted environment by using recombinant E. coli : a review. Biotechnol Environ 1 , 8 (2024). https://doi.org/10.1186/s44314-024-00008-z

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Environmental pollution and its remediation are one of the major problems around the globe. Broad varieties of pollutants viz. pesticides, hydrocarbons, heavy metals, and dyes, etc. are the key players, which are mainly responsible for environmental pollution. Residual contaminants are also difficult to eliminate. Bioremediation is one of the most efficient technologies for the reduction of environmental pollutants that recovers the contaminated site back to its actual form. So far only a small number of microbes (culturable microbes) have been exploited and a huge microbial diversity is still unexplored. To enhance the metabolic potential of the microbes, ecological restoration and degradation of recalcitrant pollutants, various bioremediation approaches like chemotaxis, biostimulation, bioaugmentation, biofilm formation, application of genetically engineered microorganisms, advanced omics, have been widely used. In the last few years, the metabolic potential of microbes has tremendously improved the realization of degradation and remediation of environmental pollution. Microorganisms help in the restoration of contaminated habitats by cleaning up waste in a environmentally safe manner along with the production of safe end products. This review discusses the important processes involved in enhancing bioremediation and recent advances in microbes and plants associated bioremediation.

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Acknowledgements

Authors are thankful to the Department of Zoology, Kumaun University, SSJ Campus, Almora (Uttarakhand), India and for providing facility and space for this research work.

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Veni Pande and Satish Chandra Pandey contributed equally to this study.

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Veni Pande, Satish Chandra Pandey, Diksha Sati & Mukesh Samant

Department of Biotechnology, Kumaun University, Bhimtal Campus, Bhimtal, Nainital, 263136, Uttarakhand, India

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Pande, V., Pandey, S.C., Sati, D. et al. Bioremediation: an emerging effective approach towards environment restoration. Environmental Sustainability 3 , 91–103 (2020). https://doi.org/10.1007/s42398-020-00099-w

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Recent Advances in Enzymes for the Bioremediation of Pollutants

Seyyed mojtaba mousavi, seyyed alireza hashemi, seyed mohammad iman moezzi, navid ravan, ahmad gholami, chin wei lai, wei-hung chiang, navid omidifar, khadije yousefi, gity behbudi.

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Academic Editor: Néstor Gutiérrez-Méndez

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Received 2021 Jan 26; Revised 2021 May 5; Accepted 2021 Jun 9; Collection date 2021.

This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Nowadays, pollution of the environment is a huge problem for humans and other organisms' health. Conventional methods of pollutant removal like membrane filtration or ion exchange are not efficient enough to lower the number of pollutants to standard levels. Biological methods, because of their higher efficiency and biocompatibility, are preferred for the remediation of pollutants. These cost-effective and environment-friendly methods of reducing pollutants are called bioremediation. In bioremediation methods, enzymes play the most crucial role. Enzymes can remedy different types of organic and inorganic pollutants, including PAHs, azo dyes, polymers, organocyanides, lead, chromium, and mercury. Different enzymes isolated from various species have been used for the bioremediation of pollutants. Discovering new enzymes and new subtypes with specific physicochemical characteristics would be a promising way to find more efficient and cost-effective tools for the remediation of pollutants.

1. Introduction

The widespread use of chemicals in industries and militaries, inadequate waste disposal, and accidental leakage cause contamination of soil, water, and air. For instance, there are 34,000 contaminated sites just in Europe that need to be treated. These pollutants are hazardous for humans, other living beings, and even the biogeochemical cycle. Pollutants' stability, low solubility, and resistance to various physical, chemical, and biological degradation pathways are the main reasons for their toxicity [ 1 ].

Different physical and chemical methods for cleaning up pollutants have been used, such as oxidizing agents, electrochemical treatments, adsorption of pollutants, ion exchange, and membrane filtration [ 2 ]. Despite the adequacy of traditional methods for the high concentration of pollutants, they were not enough for lowering the amount of contamination to regulatory limits [ 3 ]. Various disadvantages of traditional methods for cleaning up pollutants include high cost, nonspecificity, and probable secondary contamination production; therefore, ecofriendly and biological methods, called bioremediation, gained interest [ 4 ].

Bioremediation is defined as processes and products that are cost-effective and practical to minimize pollutants in the source and diminish danger to the environment and human health [ 5 ]. Its main ways of degrading and detoxifying pollutants are through intracellular accumulation or enzymatic transformation [ 4 ]. Pollutant properties (i.e., chemical structure, hydrophobicity, and polarity), environmental conditions (i.e., temperature, pH, and redox condition), and soil features (i.e., aggregation, thickness, dissolved organic matter, and pollutants aging) affect biological degradation and contaminants availability [ 6 ].

Enzymes are the most efficient bioremediation tools and progress all chemical changes on pollutants. Enzymes' specificity is usually broad enough to act on different molecules with similar structures. Moreover, it is possible to engineer the enzymes for enhancing their stability and efficiency for special conditions or particular substrates [ 7 , 8 ]. Omics technologies have a significant role in these developments [ 2 ].

Using enzymes in bioremediation could be either individually that the isolated enzyme used and added to the contaminated area or as a whole cell, e.g., bacteria, fungi, or algae. In a second way, continuous aeration, inoculation, and nutrition are necessary. Besides, environmental conditions should be prepared for microorganisms living, even though there might still be some toxic compounds in the environment that inhibit microorganisms' activity [ 1 , 9 ]. The use of individual enzymes has some advantages in comparison with microbial whole cell including greater specificity, more straightforward handling and storage, standardizable activity, more mobility as a result of smaller size, being active in the presence of high concentrations of toxic compounds, and biodegradability that inhibits persistence and recalcitrance [ 1 , 10 , 11 ]. This approach is much more efficient for extracellular enzymes and cofactor-independent enzymes [ 12 , 13 ].

Enzyme production in the natural environment is low, while it is possible to increase the produced enzyme under controlled conditions. On the other hand, recombinant DNA technology and gene engineering provide many opportunities to produce more efficient and more enzymes [ 14 ]. Moreover, nanotechnology offers some tools to increase enzymes' stability by decreasing sensitivity to mechanical stress, preserving the third structure of enzymes, and protecting them against proteases [ 9 ].

Enzymatic bioremediation could be in situ or ex situ . In in situ methods with the least disturbance in the environment, the free or immobilized enzyme (adsorbed enzymes on mineral supports that minimize the loss of enzymatic activity) is added to the soil. This approach is less expensive because of no need for excavation and transportation of soil. Ex situ methods are feasible for highly contaminated soils with toxic pollutants or when fast action is essential. During this procedure, soil was excavated and treated in different bioreactors in the best condition for enzymes' activity [ 1 ] ( Figure 1 ).

A representative scheme of different methods of soil remediation. (a) Conventional in situ remediation. (b) Using a single-phase bioreactor for solvent extraction. (c) Using a two-phase bioreactor for solvent extraction. Adapted from [ 1 ].

Different enzymes like mono- or dioxygenases, halogenases, peroxidases, phosphotriesterases, hydrolases, transferases, and oxidoreductases from various species of bacteria, fungi, algae, and plants have been used for the bioremediation of pollutants [ 10 , 15 ]. We try to review the most essential enzymes for the bioremediation of pollutants and insight into their mechanism of action.

2. Enzymes for Organic Substrates

Large amounts of organic pollutants, including herbicides, pesticides, dyes, drugs, and plastics, pollute the air, soil, and water every year. Polymers, aromatic molecules, polycyclic aromatic hydrocarbons (PAHs), chlorinated hydrocarbons, steroids, and organocyanides are the most organic compounds that need to be cleaned up worldwide. Their stable structure is the main reason for their toxicity.

2.1. Hydrolases (EC 3)

Esterases, nitrilases, aminohydrolases, lipase, cutinase, and organophosphorus hydrolase are among the hydrolase enzymes used in the bioremediation of different chemicals such as herbicides, pesticides, organophosphorus compounds, nitrile compounds, and polymers [ 1 , 2 ]. We would review some of them shortly as follows.

2.2. Esterases (3.1)

Esterases catalyze the cleavage of ester bonds in different chemicals like organophosphorus herbicides and pesticides, diethyl glycol adipate, polyurethanes, and aromatic and aliphatic polyesters. Escherichia coli and Pichia pastoris are two bacteria that express and colonize the thermostable kind of enzymes. Moreover, a subgroup of esterases found in E. coli is active in a cold environment and can act on phthalate esters [ 2 ].

It is worth noting that the product of esterase reaction with organophosphorus compounds, 3,5,6-trichloro-2-pyridinol (TCP), is metabolized later to less toxic chemicals by aminohydrolase (EC 3.5) [ 2 ].

2.3. Nitrilases (EC 3.5.5.1)

Triple bonds between carbon and nitrogen (nitrile group) of herbicides, polymers, and plastics are hydrolyzed stereo-, regio-, or chemoselectively by nitrilases to carboxylic acid and ammonia. Many species can express these enzymes, including Streptomyces sp., Fusarium solani, Rhodococcus rhodochrous, Aspergillus niger, Bacillus pallidus, and Pseudomonas fluorescens . Moreover, an evolution approach on Alcaligenes faecalis tends to isolate a nitrilase that was active in the broader range of pH. Besides, P. fluorescens nitrilase's gene expressed in E. coli is probably the most hopeful nitrilase [ 16 , 17 ]. Cyanide dihydratase (EC 3.5.5) is one of the nitrilases and degrade cyanide into formate and ammonia. Pseudomonas stutzeri and Bacillus pumilus are two species that express this enzyme. Furthermore, fungal cyanide hydratase (EC 4.2.1.66), isolated from Fusarium lateritium, Neurospora crassa , and Gloeocercospora sorghi , and some other species, is another cyanide-degrading enzyme that metabolizes it to formamide [ 18 ]. These enzymes are promising for the bioremediation of wastewaters from coal coking and metal-plating baths [ 17 ].

2.4. Organophosphorus Hydrolase (EC 3.1.8.2)

Organophosphate compounds were developed and used as pesticides and in warfare and even as a drug since 1937. They are neurotoxic, and after a while, they were more than that soil microbiota could remedy all of them. Organophosphorus hydrolase (also known as phosphotriesterase) is one of the enzymes that can serve for organophosphorus compounds bioremediation. It is mostly isolated from Pseudomonas diminuta , although its fungal form is expressed in Aspergillus niger and Penicillium lilacinum . It can act on P-S, P-O, and P-F bonds. This enzyme has Zn 2+ as a cofactor in its native form, while assays showed that substitution of Co 2+ provides the most potent activity against paraoxon [ 19 ]. This enzyme has the fastest catalytic rate and is the most promising enzyme for engineering activity against organophosphates [ 20 ].

2.4.1. Peroxidases

(1) Ligninolytic Peroxidases . Ligninolytic enzymes are a family of enzymes with broad applications in bioremediation. This group of enzymes produced by white-rot fungi (WRF) is in the condition of nutrient limitation known as “ligninolytic.” Also, lignocellulosic materials can be an inducer for the production of these enzymes [ 21 ]. Due to the high nonspecificity and high nonstereoselectivity of these enzymes, they can degrade a wide range of recalcitrant compounds [ 22 ]. They degrade chemicals by pseudo-first-order kinetic via a free-radical-based chain reaction using H 2 O 2 and molecular oxygen [ 21 – 24 ].

Ligninolytic enzymes can be categorized into four main enzymes, including laccase (LAC), lignin peroxidase (LiP), manganese peroxidase (MnP), and versatile peroxidase (VP).

(2) Laccase . For oxidizing phenolic compounds, PAHs, dyes, and pesticides benzenediol: oxygen oxidoreductase, known as laccase, is a suitable enzyme. As an oxidase, laccase substrates go through one of the following pathways: (1) cleavage of aromatic rings, (2) polymerization, and (3) degradation of covalent bonds between monomers. Four atoms of copper are the principal part of the reaction, and oxygen is the last electron receptor [ 2 , 25 ]. The mechanism of the reaction is shown in Figure 2 .

General reaction mechanism of bacterial laccases. Adapted from [ 26 ].

Laccase is first discovered in different fungi species like Panus conchatus and Polyporus sp. Later on, laccase was found in Azospirillum lipoferum, as the first bacteria species. Laccase is produced in different Gram-positive bacteria, including Bacillus , Geobacillus, Aquisalibacillus, Lysinibacillus, Staphylococcus , and Streptomyces . Many bacteria produce laccase extracellularly, while some others are unable to secrete the enzyme. Bacterial laccase is more resistant to extreme temperature and pH conditions [ 1 , 25 ].

There are two kinds of laccase, white and blue. The main difference between these is that blue laccase is dependent on a “mediator” for the degradation of nonphenolic substrates. “Mediator” is an intermediator that laccase oxidizes and turns into oxidized radicals that react with high redox potential or bulky substrates. ABTS (2,20-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid)) and N-heterocycles with N-OH such as violuric acid, N-hydroxybenzotriazole, and N-hydroxy-N-phenylacetamide have been used as effective mediators [ 25 ].

Every year, approximately 7 × 10 4 − 1 × 10 7 tons of dyes penetrate the environment [ 25 ]. Laccase is used for dyes remediation. As an example, a Bacillus licheniformis LS40-derived laccase can decolorize azo, indigo, and anthraquinone dyes by 80% within one hour in the presence of acetosyringone as a mediator [ 27 ].

PAHs are xenobiotic pollutants because of their low solubility and degradation rate. Laccase can convert PAHs to their less toxic quinine form and CO 2 . There are some examples in Table 1 . Notably, laccase can degrade some drugs such as diclofenac and mefenamic acid in acidic pH [ 25 ].

Examples of laccase's pollutant bioremediation.

(3) Lignin Peroxidase . Lignin peroxidases (LiPs) are a group of heme-containing monomeric enzymes. Their weight ranges between 38 and 43 kDa [ 30 , 31 ] with iron in the ferric state [ 21 , 32 ]. LiPs with their high redox potential [ 32 ] are capable of breaking alpha and beta carbon bonds, catalyzing the degradation of phenolic and nonphenolic compounds, demethylation, and opening aromatic ring of dyes [ 33 ]. LiPs have a high redox potential for oxidizing nonphenolic structures [ 31 ].

LiP activity increases in the presence of H 2 O 2 as an electron acceptor. However, high concentrations of H 2 O 2 could damage the LiPs [ 32 ]. In the first step of the reaction, Fe 3+ binds to H 2 O 2 and oxo-ferryl intermediate named compound I forms. Then, compound I, by a donation of one electron from the substrate, reduces to compound II, finally; by another electron donation from the substrate, iron in heme returns to its ferric resting state, and the enzyme renews to its initial form [ 31 , 34 ]. In this three-step reaction, the reduction of compound II is the rate-limiting step ( Figure 3 ) [ 36 ]. Due to this slow reduction rate, compound I is available for reaction with H 2 O 2 and the formation of a complex between LiP and superoxide (compound III) inactive enzyme [ 36 ].

Lignin peroxides catalytic reaction. Adapted from [ 35 ].

Veratryl alcohol is a secondary metabolite that can play essential roles in this oxidizing reaction. Veratryl alcohol can be the mediator in the electron transfer reaction; it can play a role in the catalytic cycle of LiP by an oxidizing terminal substrate. Vertaryl alcohol can also prevent the formation of compound III and, if compound III is established, reduce it to its native form [ 36 ].

Many WRFs produce LiPs such as Phanerochaete chrysosporium , Trametes versicolor , Bjerkandera adusta , Phlebia radiate , and Ganoderma lucidum [ 22 , 31 ].

Many technologies have been applied to enhance activity and increase catalytic characteristics of LiPs, such as LiP entrapment in calcium beads [ 37 ].

(4) Manganese Peroxidase . Manganese peroxidases (MnPs) are heme-containing glycol proteins with weight ranging from 32 to 62.5 kDa [ 38 ]. Like other ligninolytic peroxidases, MnP uses H 2 O 2 . By using H 2 O 2 , MnP can oxidase Mn 2+ to Mn 3+ . The first step of the reaction is binding an oxygen atom of H 2 O 2 to Fe 3+ of heme. Then, by two-electron transfer from Fe 3+ to peroxide Fe 4+ oxo-porphyrin, compound I radical forms. Then, compound I binds to monochelated Mn 2+ and Mn 3+ and compound II forms. Finally, by oxidizing another Mn 2+ to Mn 3+ , compound II reduces and the enzyme with Fe 3+ reforms ( Figure 4 ) [ 32 , 36 ].

Manganese peroxidase catalytic reaction. Adapted from [ 35 ].

Aliphatic organic acids such as lactate and oxalate can induce Mn 2+ oxidation rate, and Mn 3+ -acid chelates have a higher redox potential. MnP activity increases in the presence of glutathione and unsaturated fatty acids, such as tween 80. Many techniques have been utilized to immobilize and enhance the efficacy of bioremediation with MnP, such as making calcium alginate beads and carbon nanotubes [ 39 – 41 ].

MnP can remediate PAHs and nitroaromatic compounds [ 36 , 42 ], azo dyes [ 43 ], and endocrine-disrupting chemicals such as bisphenol A and alkylphenols [ 44 , 45 ]; moreover, with the contribution of mediators such as lipid and thiyl radicals, MnP is capable of oxidizing nonphenolic structures [ 34 ].

Many species of fungi are able to produce MnP, such as Phanerochaete chrysosporium , Trametes versicolor , Irpex lacteus , Dichomitus squalens , and Ganoderma lucidum [ 45 , 46 ].

(5) Versatile Peroxidase . Versatile peroxidase (VP) is a heme-containing ligninolytic enzyme considered as a hybrid between LiP and MnP. VP has two active sites; therefore, it can oxidize both Mn 2+ and veratryl alcohol by a similar mechanism to MnP and LiP, respectively [ 32 , 47 ].

VP can oxidize both low and high redox potential compounds, polycyclic aromatic hydrocarbons, azo dyes, high molecular weight aromatics, and both phenolic and nonphenolic compounds and environmental pollutants [ 32 , 47 , 48 ].

VP production is less common in WRFs than MnP and LiP, but it can be found in some species such as Pleurotus spp. and Bjerkandera spp. [ 32 ].

2.4.2. Horseradish Peroxidase

Horseradish peroxidase (HRP) is an enzyme traditionally extracted and isolated from the root of horseradish ( Armoracia rusticana ). The most abundant isoenzyme found in the root of horseradish is C isoenzyme (HRPC). HPRC is 44 kDa heme-containing glycopeptide with 308 amino acids, an iron atom in the ferric state in protoporphyrin IX, and two calcium atoms in the central zone [ 49 – 51 ]. HRP catalyzes oxidative reaction using H 2 O 2 . In the presence of H 2 O 2 , the intermediate compound formed via two-electron oxidation. Then by an oxidable substrate, compound I reduces to compound II. Radical formation occurs via these reactions, and finally, the initial enzyme can be renewed by the reaction of compound II with another substrate molecule. In comparison with LiP compound, I and II are more electronegative in HRP ( Figure 5 ) [ 52 ].

Horseradish peroxidase catalytic cycle. Adapted from [ 52 ].

HRP is applicable for removing and remediating phenols, substrate phenols, and alkylphenols, aromatic amines [ 53 , 54 ], azo dyes [ 55 , 56 ], endocrine-disrupting compounds [ 54 ], and many other environmental pollutants.

Many techniques have been utilized to immobilize and enhance the efficacy of enzyme by nanotechnology [ 57 – 59 ]. Using horseradish root is a standard method; using fertile soil for horseradish cultivation to feed the population has raised concern in recent years [ 60 ]. To solve this problem and enhance the efficacy of the enzyme, many biotechnological methods have been experienced, such as recombinant production of HRP in E. coli , yeast, plants, and insect systems [ 61 ].

2.5. Cytochrome p450 Monooxygenase (EC 1.14.14.1)

Cytochrome p450 monooxygenases (CYP) are a family of heme-containing enzymes that catalyze different reactions such as N-hydroxylation, N-dealkylation, O-dealkylation, oxidative dehalogenation, and hydroxylation of C-H bonds. CYP derives essential electrons for reactions from NADPH-cytochrome p450 reductase, and the latter enzyme derives electrons from atmospheric oxygen. So, the presence of a reducing agent like NAD (P) H or FAD is necessary [ 62 ]. The reaction cycle of CYP450 is shown in Figure 6 .

Cytochrome p450 reaction cycle. RH: substrate; ROH: product. Adapted from [ 63 ].

CYPs are versatile enzymes expressed in various species of bacteria, fungi, plants, and animals. About 7000 different CYPs have been discovered till now. Saccharomyces, Streptomyces, Basidiomycete, Dehalococcoides, Rhodococcus, Bacillus, Escherichia, and Salmonella are among the genera that their CYPs are used for bioremediation [ 64 , 65 ].

While bacterial CYPs are attractive because of their solubility, easy and low-cost production, and self-efficiency (their electron transfer reductases, e.g., FMN, FAD, and p450 monooxygenase, are on a single peptide), mammalian CYPs are membrane-bounded, dependent on a redox partner (e.g., NADPH) and have expansive applications [ 65 ]. Bacterial and eukaryotic CYPs can oxidize aliphatic hydrocarbons with 5–16 and 10–16 carbon lengths, respectively [ 66 ]. Notably, eukaryotic CYPs need modification at N-terminal, but prokaryotic ones are active in the native form [ 64 ].

Dioxins, PCBs (polychlorinated biphenyls), PCDDs (polychlorinated dibenzo-p-dioxins), PCDFs (polychlorinated dibenzofurans), PAHs, aliphatic hydrocarbons, and even Cr (VI) are pollutants that can be degraded and bioremedied by CYPs [ 1 , 14 , 65 , 67 ]. In Table 2 , the list of different CYPs and their substrates are shown. Immobilizing CYPs can improve their activity even to 10-folds higher than free enzyme. Besides, transgenic plants that can produce special CYPs are a way toward herbicide-resistant plants [ 65 ].

Cytochrome p450 subtypes and their substrate for bioremediation.

CYPs are interesting enzymes for bioremediation because of their wide range of substrates and diverse oxidative reactions. Among the limitations of using CYPs are their dependency on expensive cofactors, low stability, and low activity [ 68 ].

3. Enzymes for Inorganic Substrates

In the presence of toxic heavy metals, most of the microorganisms produce metal-binding peptides such as phytochelatins and metallothioneins, which reduce their toxicity via sequestration [ 70 ]. For example, phytochelatin synthase is the enzyme responsible for the production of phytochelatin that, in cooperation with GSH, accumulates heavy metals [ 71 ]. Among the limitations of these metal-binding proteins is their nonselectivity. To solve this problem, many microorganisms developed specific pathways for resistance against heavy metals [ 4 ]. Obviously, enzymes are the most critical part of these pathways; we would review some of these metal-specific enzymes as follows.

3.1. Arsenic

Arsenic is a heavy metal that exists in nature in organic and inorganic forms. The inorganic forms (As 3+ (arsenite) and As 5+ (arsenate)) are toxic and may cause enzyme inactivation, carcinoma, hemolysis, keratosis, gangrene, and neurological and cardiovascular diseases [ 72 , 73 ]. Arsenate and arsenite convert to each other by arsenate reductase and arsenite oxidase through redox reactions. As 3+ is more mobile and toxic. As 5+ is the terminal electron acceptor in the absence of oxygen and reduces to As 3+ [ 63 ]. Ferredoxin or glutathione would be the electron source [ 74 ]. This process enhances the solubility of As and eases leaching from soil [ 73 ]. The final As 3+ is excreted through efflux pumps, ArsB and Acr3 [ 74 ]. Arsenite oxidase converts As 3+ to less toxic As 5+ to be used either for a supplemental energy source or as an electron donor for CO 2 fixation [ 74 ]. The final arsenate is immobile and would be retained by sediments [ 73 ].

The methylated form of arsenic is volatile and would be lost from the soil [ 73 ]. Interestingly, in methanogenic bacteria, As methylation is coupled with methane biosynthesis and can detoxify soil through this mechanism. Coenzyme M is the biocatalyst of this detoxification process [ 63 ].

Many species can remedy As in different ways. The bacterial ones include Acinetobacter sp., Pseudomonas sp., and Sporosarcina ginsengisoli [ 75 ]. E. coli, Bacillus idriensis , and Sphingomonas desiccabilis are engineered species for As bioremediation [ 72 ]. Some fungi, including Rhizobium sp., Rhizopus sp. , Trichoderma sp., Aspergillus flavus , and Penicillium canescens , are As bioremediators too [ 63 , 73 ]. Moreover, some yeasts like Saccharomyces cerevisiae can reduce arsenate by ArsC ( Figure 7 ), a protein that has As reductase activity. Algae genera, like Hydrodictyon, Oedogonium, Rhizoclonium, and even a plant, Pteris vittata from Pteridaceae, have the potential to be used for bioremediation [ 75 ].

A strategy used for arsenic detoxification using E. coli and S. cerevisiae and their enzymes. Adapted from [ 63 ].

Lead was found in a small amount in nature before industrialization. However, now, through gasoline burning, different Pb salts originate in and contaminate water, soil, and air [ 72 ]. Lead toxicity may cause anemia and appetite loss and gastrointestinal, neurological, and reproductive disorders [ 73 ]. Organoleads, especially tetraethyl lead and tetramethyl lead used in gasoline, are toxic forms of lead. They are sensitive to photolysis and volatilization and degrade to dialkyl species. Though, some bacteria can degrade organoleads through bioremediation processes [ 76 ].

Cupriavidus metallidurans can remove Pb 2+ ions with p-type ATPase and produce inorganic phosphate to sequester Pb 2+ in the periplasm [ 76 ]. Staphylococcus epidermidis can biomineralize Pb 2+ by carbonate. Urease enzymes form different carbonate crystalline Pb 2+ . It can be mineralized as oxalate and pyromorphite, too [ 77 ]. Agaricus bisporus, Rhizopus nigricans, Penicillium canescens, Penicillium chrysogenum, Saccharomyces cerevisiae, Aspergillus niger, and Aspergillus terreus are among biotransforming organisms [ 72 , 73 ]. Moreover, it is reported that Arthrobacter and Phaeolus schweinitzii can degrade trimethyl lead cations [ 78 ].

3.3. Mercury

Mercury is a heavy metal that is toxic in both organic and inorganic forms, although the organic form is more toxic. Hg toxicity would cause neurotoxicity, nephrotoxicity, allergies, and inability to speak [ 73 , 79 ]. Hg is a rare element in Earth crust, but it spreads and pollutes soil and water because of different humic activities like gold mining, various measurement tools (barometer, thermometer, manometer, etc.), lamps, mercurial fungicides, paper manufacturing industry, and battery cells [ 72 ]. Its environmental cycle is shown in Figure 8 .

Mercury cycle in the environment. Adapted from [ 80 ].

Mercury exists in three forms: metallic mercury (Hg 0 ), mercurous (Hg +1 ), and mercuric (Hg 2+ ) forms. The most toxic form of Hg is mercuric chloride. Organic mercury can accumulate in living organisms and has an affinity for proteins' sulfhydryl groups. Inorganic mercury has the lowest toxicity because of its low solubility and high vapor pressure. Mercury-resistant bacteria (such as Pseudomonas, Aeromonas, Staphylococcus, Escherichia, Citrobacter, Bacillus, and Rhodococcus ) can reduce toxic organic forms of Hg to less toxic metallic Hg. Mercuric reductase is the main enzyme that reduces Hg. The mer operon is the collection of mercury-resistance genes activated in the presence of an inducible concentration of Hg. Mercuric reductase in cooperation with FAD and NADPH, as electron sources, reduces Hg 2+ to Hg 0 . The final metallic mercury is volatile and spreads to the atmosphere [ 80 , 81 ]. Also, dimethylmercury is volatile and biomethylation can serve as a strategy for Hg bioremediation [ 73 ]. The mer operon-independent volatilization of mercury has been discovered, too, in Shewanella oneidensis [ 82 ].

Another enzyme that plays a role in mercury bioremediation is organomercurial lyase that breaks the carbon-mercury bonds in organo-Hg compounds [ 80 , 81 ].

Various microorganisms such as Rhizopus arrhizus, Penicillium canescens, Geobacter sulfurreducens, Pseudomonas putida, Acinetobacter calcoaceticus, Staphylococcus aureus, and Shigella flexneri can remedy mercury [ 72 , 80 ]. Enterobacter, Pseudomonas , and Bacillus are the most used genera for this purpose [ 83 ].

3.4. Chromium

Cr (VI) is the most toxic heavy metal because of its high oxidative potential causing cell damage and mutagenic, carcinogenic, and teratogenic effects [ 84 ]. The wide use of chromium and its compounds and mining exerts this pollutant to waters and soils. Bioremediation of hexavalent chromium is through reduction to trivalent species. Pseudomonas, Bacillus, Escherichia, Shewanella, Enterobacter , and Thermus are some genera that are resistant to Cr (VI) and can reduce it. The reduction of hexavalent chromium may occur through aerobic or anaerobic pathways [ 14 ]. In the anaerobic process, soluble cytoplasmic enzymes are involved and reduce hexavalent chromium in two steps. In the aerobic reduction of chromium, usually, Cr (VI) is a terminal electron acceptor, while in different species, NADPH, NADH, or formate serves as an electron donor. Chromate reductase, Ni-Fe dehydrogenase, and cytochrome c3 are among the enzymes reported to have hexavalent chromium-reducing activity [ 85 ]. Also, Fe 2+ and S 2- produced in some bacteria can reduce Cr 6+ even faster than chromate-reducing bacteria. The detailed mechanism of chromate resistance in bacteria is shown in Figure 9 .

Chromate resistance mechanism in bacteria. (A) Mutation in sulfate uptake transporters. (B) Extracellular reduction of Cr 6+ to Cr 3+ . (C) Intracellular reduction of Cr 6+ to Cr 3+ by chromate reductase. (D) Reducing oxidative stress and activation of repairing systems. (E) Outflowing of chromate from the cytoplasm. (F) Decreasing oxidative stress by activation of ROS scavenging enzyme. Adapted from [ 14 ].

Nitroreductase, iron reductase, flavin reductases, and quinone reductases are bacterial enzymes that reduce Cr 6+ [ 86 , 87 ]. Mammals reduce this pollutant, too, by CYP, aldehyde oxidase, and DT-diaphorase. Some of these bacterial enzymes are extracellular, including nitrate reductases, flavin reductases, and ferrireductases [ 14 ].

4. Conclusion

In this review, we aim to provide an insight into the role of the enzyme in the bioremediation of pollutants. While many physical and chemical methods of treating contaminated soil and water are not efficient enough, bioremediation opens a new way to clean up toxic pollutants. Enzymes as practical tools of living organisms are an ecofriendly and bio-based strategy for bioremediation. Microorganisms exposed to contaminated sites and specific pollutants are fascinating sources for the isolation of active enzymes against those pollutants. Interestingly, we may find some enzymes in completely irrelevant places to pollutant sources. Discovering TCP-degrading enzymes and chlorpyrifos-degrading enzymes in the cow rumen microbiome is an instance for this claim [ 2 ].

Overall, using enzymes for pollutant bioremediation seems to be a cost-effective, efficient, and practical approach. Although there are still many ways to go, further studies and experiments on enzyme activity and mechanism of action and isolating new enzymes would be a promising way to reduce pollutants and make a healthier environment for humans and all other species.

Contributor Information

Ahmad Gholami, Email: [email protected].

Chin Wei Lai, Email: [email protected].

Wei-Hung Chiang, Email: [email protected].

Data Availability

The data used to support this study are available upon request.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

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REVIEW article

Bioremediation of environmental wastes: the role of microorganisms.

• 1 Food Security and Safety Focus Area, Faculty of Natural and Agricultural Sciences, North-West University, Mmabatho, South Africa
• 2 Department of Biological Sciences, Kings University, Ode-Omu, Nigeria
• 3 Environmental Pollution Science and Technology, (ENPOST), Ido-Ijesha, Ilesha, Nigeria

The growing rate of urbanization and industrialization has led to an increase in several types of pollution caused by the release of toxic chemicals to the environment. This is usually perpetuated by the manufacturing industry (e.g. detergent and dye), agricultural sectors (e.g. fertilizers and pesticides), mining industry (e.g. cyanide and sulphuric acid) and construction companies (e.g. cement and metals). These pollutants have adverse effects on the health of plants, animals, and humans. They also lead to the destruction of the microbial population in both aquatic and the terrestrial regions, and hence, have necessitated the need for remediation. Although different remediation methods, such as the physical and chemical methods, have been adopted for years, however, the drawbacks and challenges associated with them have promoted the use of an alternative which is bioremediation. Bioremediation involves using biological agents such as plants and microbes to remove or lessen the effects of environmental pollutants. Of the two, microbes are more utilized primarily because of their rapid growth and ability to be easily manipulated, thus enhancing their function as agents of bioremediation. Different groups of bacteria, fungi and algae have been employed to clean up various environmental pollutants. This review discusses the types, mechanisms, and factors affecting microbial bioremediation. It also recommends possible steps that could be taken to promote the use of microbes as bioremediation agents.

1 Introduction

The rise of urbanization and industrialization, has left the environment exposed to numerous pollutants which are toxic to living things. Pollutants arising from different industrial processes are major sources of pollution to the soil and aquatic environment. Different types and quantities of heavy metals are released during the industrial production process and as effluents after further industrial production. For instance, the wastewater from dye-producing companies are associated with antimony, chromium and mercury ( Methneni et al., 2021 ). The application of fertilizers, pesticides and herbicides in the agricultural sector generates pollutants that include aluminium, copper, zinc, nickel, lead and arsenic to the environment ( Ayilara et al., 2020 ; Prabagar et al., 2021 ). Similarly, untreated pollutants from wastewaters of the agri-food industries disposed into river canals and other waterbodies have harmful effects on the environment ( Siric et al., 2022a ; AL-Huqail et al., 2022 ). Crude oil also serves as a major environmental pollutant particularly through pipeline vandalization, transportation leakage, and/or accidental spillage ( Ogunlaja et al., 2019 ). During mining, some chemicals such as lead, arsenic, cadmium, and copper which are toxic to the immediate environment are released ( Liu et al., 2020 ). Some other environmentally toxic chemicals including but not limited to cyanide and sulphuric acid are used during the mining process. ( Ayangbenro et al., 2018 ; Orlovic-Leko et al., 2022 ). Equally, other industrial wastes such as those produced in cement-making industries release zinc, copper and cadmium and can be found in the top soils ( Jafari et al., 2019 ). Chromium and lead from pharmaceutical effluents ( Kumari and Tripathi, 2020 ), plastics containing lead, manganese, iron, copper, chromium, silver, cadmium, antimony and mercury all pollute water ( Zhou et al., 2019 ). In addition, copper, arsenic, mercury, chromium, lead, nickel, cadmium and zinc from the coal industry serve as environmental pollutant ( Sun et al., 2019 ). These heavy metals are very toxic to aquatic and terrestrial habitats and their inhabitants. In humans, mercury, cadmium and lead alters the central nervous system, especially in infants, while lead results in liver and kidney dysfunction, cardiovascular diseases, malfunctioning of the reproductive and immune system ( Zwolak et al., 2019 ; Fashola et al., 2020a ; Fashola et al., 2020b ; Ayangbenro and Babalola, 2020 ). Cadmium causes cancers, skeletal disorders, neurotoxic and nefrotoxic complexities, and dysfunction of the reproductive system ( Zwolak et al., 2019 ; Fashola et al., 2020a ; Fashola et al., 2020b ; Ayangbenro and Babalola, 2020 ). Wastes containing heavy metals are often improperly disposed into soil and water environments. When disposed into water bodies, they can lead to the death of fishes, and other aquatic inhabitants, otherwise, they are biomagnified and cause chronic diseases in humans and animals. Therefore, there is need for the remediation of these pollutants using physical, chemical, or biological methods. The physical and chemical methods have been used for years but they come with their drawbacks which include the need for an expert and special equipment for the chemical bioremediation procedure while the physical bioremediation procedure is expensive ( Mahmood et al., 2021 ). This has called for the need for a better alternative which is the biological remediation (Bioremediation). Bioremediation is a most efficient, eco-friendly and cost effective technology for the transformation of contaminants ( Sonune, 2021 ). Biological remediation can be carried out using both plants and microorganism, nonetheless, plants take a longer time to grow and cannot be easily manipulated like the microbes which makes the microbes more preferable ( Hussain et al., 2022 ). In addition, microbes mitigates heavy metals and improve soil fertility and plant development ( Chaudhary et al., 2023b ). Hence, this review discusses the types, mechanism, challenges as well as the factors affecting microbial bioremediation, with recommendation on how to enhance the use of microbes in aquatic and terrestrial bioremediation.

2 Different pollutants and their toxicity on living things

Exposure of humans to air pollutants can cause developmental disorders, respiratory problems, cancers, cardiovascular diseases, and other health issues ( Table 1 ). For instance, it has been reported that exposure to particulate matter in the air was associated with an increased risk of premature death in humans ( Pope et al., 2019 ). Nitrogen oxides produced by combustion processes, are significant air pollutants. They irritate the respiratory system, cause cough, shortness of breath, and exacerbate asthma ( Zhao et al., 2020 ). Equally, Sulfur dioxide, produced by burning fossil fuels, can cause respiratory and cardiovascular diseases, including bronchoconstriction, shortness of breath, and coughing. A recent study found that exposure to sulfur dioxide was associated with increased mortality from respiratory diseases in China ( Luo et al., 2015 ). Volatile organic compounds (VOCs), emitted by various sources, including paints, cleaning products, and vehicle emissions, can cause eye, nose, and throat irritation, headaches, nausea, and dizziness. Some VOCs (such as benzene) are also carcinogenic, and are associated with an increased risk of leukemia ( Bala et al., 2021 ). Water pollutants which include pesticides, heavy metals, and organic compounds are sometimes ingested by humans either directly or indirectly (through the consumption of aquatic animals). These pollutants can cause various health problems, including cancer, neurological disorders, and reproductive issues. It has been reported that exposure to heavy metals result in a higher risk of hypertension and kidney damage in humans ( Wu et al., 2018 ; Rai et al., 2019 ).

Table 1 Effect of pollutants on living things.

Similarly, different animal diseases are caused by pollutants. Exposure to particulate matter (PM) can cause inflammation and damage to the respiratory system of animals, leading to respiratory diseases such as chronic obstructive pulmonary disease (COPD) and asthma ( Manisalidis et al., 2020 ). When animals consume water contaminated with heavy metals, pesticides, and pharmaceuticals, it leads to reproductive disorders, liver damage, and cancer ( Hitt et al., 2023 ). Nitrogen dioxide when present in the environment, reduces the growth of plants and the yield of crops while sulfur dioxide causes acid rain and acidification ( Manisalidis et al., 2020 ). An impairment in the photosynthetic rhythm and metabolism is observed in plants exposed to ozone ( Zuhara and Isaifan, 2018 ). In the aquatic environment, eutrophication occurs when there is a high concentration of nitrogen availability. This leads to algal bloom and cause death and disequilibration in the diversity of fish ( Zuhara and Isaifan, 2018 ).

2.1 Types of remediation

There are different types of remediation, namely the physical, chemical and biological techniques. The physical remediation involves the use of skimmers, sorbent materials and booms. Boom is a physical barrier made of materials that absorbs oil pollutants and prevents it from spreading before a further remediation procedure is carried out ( Vocciante et al., 2019 ) ( Figure 1 ). Skimmers and sorbents are methods that are further used to absorb and adsorb pollutants after booms ( Kumari et al., 2019 ). The major challenge associated with the use of bloom remediation technique is that it is dependent on the buoyancy and roll response. When the boom is buoyant, it floats and remains longer on the water surface. The roll response refers to the torque required to rotate the bloom from its vertical position. That is, an increased roll response results in a higher remediation process ( Dhaka and Chattopadhyay, 2021 ).

Figure 1 Types of bioremediations.

Chemical remediation is the process of adding chemicals such as clay minerals, phosphate, biochar, aluminum salts, silicocalcium materials, and sulfide to stabilize and remove heavy metals from the environment. The mechanism behind the use of these chemicals include adsorption, reduction, oxidation, complexation, precipitation and ion exchange ( Xu et al., 2022 ). Chemical remediation technique is an easy, simple, and rapid technique; however, the chemical used can also serve as a source of environmental pollution ( Xu et al., 2022 ) ( Figure 1 ).

Bioremediation is another method of pollution treatment, it is a sustainable, affordable and safe remediation technique ( Kumar A. et al., 2021 ; Kumar G. et al., 2021 ; Patel A. K. et al., 2022 ). The technology involves the use of organics such as plants and microbes. The viability of this method depends on the nature, location and level of pollution ( Patel A. K. et al., 2022 ). Microbes on the other hand have proved to be efficient in the remediation of environmental pollutants. They are preferred to plants in remediation, this is due to their ease of growth, rapid growth period and easy manipulation. It is therefore necessary to improve the use of microbes as agent of bioremediation to promote a sustainable environment.

3 Different microbes used as bioremediation agents

Microorganisms can convert toxic elements into water, carbon dioxide, and other less toxic compounds, which are further degraded by other microbes in a process referred to as mineralization ( Mahmoud, 2021 ; Kumar G. et al., 2022 ). Bioremediation can be carried out using bacteria, fungi, algae, etc. ( Table 2 ). Microbes are ubiquitous in nature, and they utilize a wide range of substrates as carbon source; hence, they are found in unusual environments where they can absorb a wide range of pollutants ( Kour et al., 2022 ). Also, their ability to survive in odd environments promote their efficiency. For example the acidophiles survive in acidic environments, the psychrophiles thrive in cold climates and the halophiles survive in saline region ( Perera and Hemamali, 2022 ).

Table 2 Different microbes used in bioremediation.

4 Mechanisms of microbial bioremediation

Microbes can remove pollutants from the environment using different mechanisms. These mechanisms can be placed into two broad categories namely immobilization and mobilization ( Ndeddy Aka and Babalola, 2016 ; Verma and Kuila, 2019 ). Mobilization process involves, enzymatic oxidation, bioleaching, biostimulation, bioaugmentation and enzymatic reduction procedure. On the other hand, immobilization includes bioaccumulation, complexation, biosorption, and precipitation (solidification) ( Tak et al., 2012 ; Ayangbenro et al., 2019 ). During mineralization, microbes help transform pollutants into end products such as carbon dioxide and water or other intermediate metabolic substances. Similarly, immobilization is the conversion of compounds into a form where it will be unavailable in the environment. For instance, the conversion of nitrate nitrogen into organic nitrogen ( Pratush et al., 2018 ). The method is usually utilized for the bioremediation of heavy metals, especially in highly contaminated environments.

Immobilization can be carried out using the in-situ and the ex-situ methods ( Pratush et al., 2018 ). The ex-situ process involves the removal of polluted soils from the site of pollution to another location where it would undergo a microbial process to immobilize the metal ions responsible for the contamination ( Ayangbenro and Babalola, 2017 ). On the other hand, in the in-situ procedure, the pollution is treated on site ( Cao et al., 2020 ). Microbes such as E. asburiae and B. cereus have been reported to be involved in immobilization of heavy metals which pollute the environment ( Fashola et al., 2020a ). During microbial bioremediation, microbes protect themselves from toxic compounds by forming hydrophobic or solvent efflux pump that protects the outer membrane of the cell ( Verma and Kuila, 2019 ).

4.1 Enzymatic oxidation

Enzymatic oxidation is the process of oxidizing pollutant compounds from a higher oxidation state to a lower one, during which heavy metals lose an electron and become less toxic. This process utilizes an enzyme (oxidoreductase) released by the microbes involved. This method is highly effective in the remediation of dyes, phenols, and other pollutants which are not easily degraded by bacteria ( Unuofin et al., 2019 ). The oxidative enzymes form radicals which can be broken down into different fractions, eventually forming compounds with high molecular weight ( Unuofin et al., 2019 ). An example of an oxidoreductase enzyme is laccase, which catalyzes the oxidation of aromatic amines ( Gangola et al., 2018 ). Other examples are phenols and polyphenols, which cause the reduction of molecular oxygen to water ( Kushwaha et al., 2018 ; Sahay, 2021 ). Laccase production has been reported in Pycnoporus sp. and Leptosphaerulina sp. where it was outlined to degrade heavy metals ( Copete-Pertuz et al., 2018 ; Tian et al., 2020 ).

4.2 Enzymatic reduction

This process is the opposite of enzymatic oxidation, here, the pollutants are converted to a reduced oxidized state where they become insoluble. Obligate and facultative anaerobes carry out the process; this method is effective in the bioremediation of compounds such as polychlorinated dibenzo-p-dioxins and dibenzofurans ( Zacharia, 2019 ). Equally, chrome reductase catalyzes the reduction of hexavalent chromium to trivalent chromium, and azoreductase reduces the azo compounds by cleaving to azo bonds ( Saxena et al., 2020 ). Much more research is needed to unravel other organisms which are capable of bioremediating pollutants in the environment.

4.3 Bioaugmentation

Microorganisms are specially added to polluted sites to feed on toxic pollutants in a process referred to as bioaugmentation. It is a very effective, rapid and cost-effective method of bioremediation ( Mahmoud, 2021 ). External microbes are added to polluted sites to augment the resident microbes. In other cases, it could also involve the isolation and genetic modification of microbes from the site of pollution before returning them to the same site for remediation. Genetic manipulation of resident microbes of polluted sites is carried out because the organisms may naturally not be capable of degrading the pollutant present at a site, and hence are modified to enhance their ability. In some other cases, non-resident microbes are added to polluted areas to promote the degradation of pollutants. The effectiveness of these new strains depends on some factors, which include the ability to compete with the resident microbes and the ability to adapt to the new environment ( Fashola et al., 2016 ; Ayangbenro and Babalola, 2017 ; Goswami et al., 2018 ; Babalola et al., 2019 ). Burkholderia sp. FDS-1 which was added to a polluted site, has been reported to degrade nitrophenolic compound present in pesticides polluted soil to a less toxic form at a slightly acidic pH and a temperature of about 30° C ( Goswami et al., 2018 ; Ojuederie et al., 2021 ) ( Table 3 ).

Table 3 Mechanism of Bioremediation.

4.4 Biostimulation

Biostimulation is the addition of nutrients (such as nitrogen, potassium, phosphorus), metabolites, electron donors, enzymes, electron acceptors, biosurfactants, etc., which are limiting to the soil to enhance the activity of the resident microbes and increase the remediation process ( Ojuederie and Babalola, 2017 ; Ayangbenro and Babalola, 2018 ). It is an affordable, environmentally friendly and efficient process ( Goswami et al., 2018 ). Compared to the bioaugmentation method, the biostimulation method is preferable because indigenous microbes are more competitive than the introduced ones ( Sayed et al., 2021 ), and this method helps to maintain the natural microbial diversity balance of the environment. Nivetha et al. (2022) reported the effectiveness of Bacillus sp., Rhodococcus sp., Staphylococcus sp., Klebsiella sp., Pseudomonas sp., and Citrobacter sp. in bioremediation of heavy metals through the biostimulation technique. Unfortunately, as effective as this method of bioremediation may be, it could lead to some other environmental complications, including eutrophication due to the excess nutrient present in the environment. Also, if the sources of the nutrients are chemicals (synthetic), they can serve as a source of pollution to the environment defeating the initial purpose of bioremediation ( Table 3 ).

4.5 Bioleaching

Bioleaching is the process of utilizing acidophilic microbes to promote the solubilization of heavy metals which are in a solid state from the sediment matrix. The process is particularly useful for iron or sulfur pollutants ( Sun et al., 2021 ; Bhandari et al., 2023 ). Therefore, iron- or sulfur-oxidizing bacteria are majorly recruited for this process; examples of such organisms are A. thiooxidans , Aspergillus sp., Mucor sp., Penicillium sp., Cladosporium sp. and Rhizopus sp. ( Medfu Tarekegn et al., 2020 ). These microbes create an acid environment and solubilize heavy metals in an immobilized state, into an aqueous solution ( Medfu Tarekegn et al., 2020 ).

4.6 Biosorption

This is the adsorption of heavy metals from pollutants through proton and ion displacement, complexation, chelation and physical interaction with electrostatic forces ( Mahmoud, 2021 ). It involves the removal of contaminants from solutions as a result of the outer cell shield of bacteria, fungi and algae which are bioremediation agents. Generally, metals are linked through the active groups of the compounds which exist at the cells surface layer. This results in the transfer of ion between metal cations and the negatively charged active group potentials present at the outer part of the microorganism structure. Rhodococcus erythropolis , Streptomyces sp. K11, and Bacillus anthracis have been reported to be capable of bioremediation through the biosorption process ( Mathew and Krishnamurthy, 2018 ; Baltazar et al., 2019 ; Sedlakova-Kadukova et al., 2019 ). Oftentimes, heavy metal pollutants (e.g., gold, zinc and copper) have some economic importance and are very useful in industrial processes. Hence, the ability of the compounds to be recovered through a process called desorption (using the solution of weak mineral solution or chelating compounds), which is a reversible step in biosorption makes it a good process ( Medfu Tarekegn et al., 2020 ).

Complexation involves using ligand to form a complex with inorganic metals, which are pollutants in the environment, especially solid wastes ( Ayangbenro and Babalola, 2017 ). Complexation is carried out mainly through different agents, namely the high molecular weight ligands, siderophores and toxic metal-binding compounds as well as the low-molecular weight organic acids (alcohols, tricarboxylic acids and citric acids) ( Pratush et al., 2018 ). Complexation occurs when extracellular polymeric substances, found on the surfaces of microbes interact with heavy metals which pollute the environment ( Xie et al., 2020 ). Xiao et al. (2019) reported the removal of copper (II) oxide and hexavalent chromium from wastewater using biochar in a mechanism which includes complexation. The organisms that have been reported to be involved in complexation include Rhodobacter blasticus ( Bai et al., 2019 ) and B.lichenformisis ( Wang et al., 2019 ).

When microbes are exposed to a polluted environment where there is iron-deficiency, they produce siderophores which are iron chelators. The siderophores have binding groups such as hydroxamate, catecholate and phenolates that form complexes with heavy metals and increase their solubility ( Khan et al., 2018 ). Siderophores are capable of producing reactive oxygen species, which also enhance their function as bioremediation agents for organic contaminants ( Albelda-Berenguer et al., 2019 ). Cyanobacteria have been reported to be effective as bioremediation agents due to the production of siderophores; for example, they are capable of bioremediating complex compounds like polythene and are capable of producing different types of siderophores, which include the anachelin, synechobactin and schizokinen ( Arstol and Hohmann-Marriott, 2019 ; Sarmah and Rout, 2020 ) ( Table 3 ).

4.7 Bioaccumulation

Bioaccumulation refers to the process where the rate of absorption of a compound is more than the rate at which the compound is lost. This process leads to the (toxic) build-up of compounds in the intracellular portion of the microbes. ( Sharma et al., 2022a ). Heavy metals move across the membrane of microbes using different mechanisms such as carrier-mediated transport, protein channel and ion pumps ( Mir-Tutusaus et al., 2018 ). Many organisms have been reported to be very active in bioaccumulation of heavy metals. For example, Rhizopus arrhizus , bioremediates mercury, Pseudomonas putida , bioremediates cadmium and Aspergillus niger bioremediates thorium ( Sharma et al., 2022a ).

4.8 Precipitation

This is the conversion of heavy metals or pollutants into precipitates or crystals, resulting in a reduced toxicity level; this process can occur during the biogeochemical cycling to form deposing of metals (iron and manganese), mineralized manganese and silver as well as microfossils, due to the activity of enzymes and galactosis of secondary metabolites ( Sharma et al., 2022a ). For instance, sulfate-reducing bacteria are capable of converting organo-phosphate to ortho-phosphate when the pH is alkaline (i.e. above 7) ( Pratush et al., 2018 ). Similarly, Bacillus subtilis and Oceanobacillus indicireducens have also been reported to be associated with the precipitation of heavy metals in the environment ( Maity et al., 2019 ).

5 Factors affecting microbial bioremediation

The ability of microbes to bioremediate heavy metals is determined by different factors, which include the total metal ion concentration, redox potential, chemical forms of the metals, competition among microbes, pH, temperature, soil structure, presence of oxygen, moisture content, nature of the soil and the solubility of the heavy metal in water ( Medfu Tarekegn et al., 2020 ). At acidic pH, free ionic species are formed by heavy metals, leading to the availability of more protons which would saturate the binding site of the metals. The pH of an environment affects the structure of the pollutant and also determines the ability of the microbe to survive in such an environment; the optimum pH that enhances bioremediation falls between 6.5 and 8.5 ( Kharangate-Lad and D’Souza, 2021 ).

Microbes compete for carbon which is a limited resource and serve as an energy source for microbes. Therefore, the inherent ability of the microbes, which compete better to degrade heavy metal pollutant, would affect the biodegradation rate. In addition to carbon, microbes responsible for biodegradation also require nitrogen (N) and phosphorus (P), thus it is important to balance the C:N:P ratio to enhance the rate of biodegradation, in environment when these essential nutrients are limited. They can be added to increase microbial activities ( Bala et al., 2022 ). The type and population of microbes determine the rate and success of a bioremediation process, for instance in the laboratory, a strain of organism might successfully bioremediate a particular heavy metal, which becomes problematic in a field situation where a consortium of microbes would be needed ( Patel A. B. et al., 2022 ). The molecular nature, gene and enzyme induction, metabolite production, growth efficiency and survival rate affect the ability of individual microbes as bioremediation agents ( Kebede et al., 2021 ). In addition, the ionization of the cell wall’s chemical moieties, the configuration of the microbial cell wall and sorption site also affect the rate of microbial biodegradation ( Mahmoud, 2021 ).

The amount of moisture present in an environment affects the solubility of the heavy metals in water, as well as their availability, pH and osmotic pressure ( Medfu Tarekegn et al., 2020 ). At a high moisture content, the microbial biodegradation rate is very low. This might be a result of an anaerobic condition that is created, which prevents the survival of aerobic microbes. Also, at a low moisture content, microbes might not be able to survive; hence an optimum moisture content is required for a successful microbial biodegradation process. In the cold regions where only psychrophiles can survive, the rate of microbial degradation of heavy metals is slow. This is because metabolic activities are reduced as the microbial transport channels is freezed by the sub-zero water; the degradation of each compound also occurs at different temperature even though most bioremediation processes are favored by high temperature ( Ren et al., 2018 ; Bala et al., 2022 ; Sharma et al., 2022c ). At an increased temperature, the rate of heavy metal solubility is increased, which consequently increases their rate of availability as well as the rate of microbial biodegradation ( Mahmoud, 2021 ).

Similarly, the chemical structure, bioavailability, concentration, toxicity and stability of the metal or pollutant determines the rate at which microbial biodegradation takes place ( Kebede et al., 2021 ). For instance, heavy metals with a simple chemical structure and low concentration would be easier to be remediated by microbes compared to those with a complex chemical structure and high temperature. Cycloalkane compounds that are highly condensed as well as high molecular weight polymatic hydrocarbons (those containing four rings and above) are more difficult to degrade compared to the lighter polyhydrocarbons (anthracene, naphthalene and phenanthrene) and unbranched alkanes (alkanes with intermediate length of about C 10 –C 25 ) ( Kebede et al., 2021 ). Hence, in order of ascending degradation, the n-alkanes are more easily degraded compared to the branched alkanes, low molecular weight aromatics, high molecular weight hydrocarbons and the asphaltenes ( Imam et al., 2019 ). Biodegradation is carried out aerobically and anaerobically. The ability of an organism which degrades a particular nutrient to survive in such an environment depends on the nature of the organism ( Jacob et al., 2018 ). For example, oxygenase associated with organisms that are active in aerobic regions is only produced in the presence of oxygen.

Different soil parameters, including the soil region, moisture-holding capacity texture and particle size, affect the rate of microbial biodegradation ( Alvarez et al., 2020 ). There is a higher population and diversity of microbes at the top layer of the soil (0-10cm). This is due to the increased availability of oxygen and organic matter, which is the opposite of what happens in sediment soils ( Ndeddy Aka and Babalola, 2017 ). In soils with fine particles, such as clayey soils, hydrocarbon retention takes place more at the surface, which renders the nutrient of the soil and oxygen unavailable. Therefore the best soil texture that promotes increased microbial biodegradation is the well-drained soil which supports oxygen availability and inhabits more soil microbes ( Huang et al., 2019 ). The presence of salinity has an effect on the hydrocarbonoclastic activity of the halotolerant and halophilic microbes, and it also exposes the soil microbes to stress conditions. The osmotic pressure of microorganisms increases as the saline concentration of an environment increases. This has a direct negative impact on the metabolic activities, of the microbes as well as the transportation system and solubility of the heavy metals ( Imron et al., 2020 ; Kebede et al., 2021 ).

6 Microbial enzymes used in bioremediation

Different microbial enzymes have been reported to be helpful in the removal of pollutants (especially heavy metals) in the environment ( Verma and Kuila, 2019 ; Bhatt et al., 2021a ; Chaudhary et al., 2023a ) ( Table 4 ). Mechanisms such as elimination, oxidation, ring-opening and reduction are used by enzymes in bioremediation ( Bhandari et al., 2021 ). Different factors which include temperature, contact time, concentration and pH affect the potency of microbial enzymes ( Bhandari et al., 2021 ). Enzyme bioremediation is expensive and time-consuming and therefore cannot be used when there is an urgent need for bioremediation ( Narayanan et al., 2023 ). Equally, the stability and activity of the pollutants, affects the potency of the bioremediation process. It is difficult to determine and discover multiple sources of a particular type of enzyme which might make the procedure unsustainable ( Narayanan et al., 2023 ).

Table 4 Enzymes used in Microbial Bioremediation.

7 Molecular approaches for validating microbial remediation

Molecular mechanisms help to unravel the microbial metabolism, genes, nature, diversity and dynamics of microbes involved in microbial remediation. Diverse molecular mechanisms are utilized in the study of microbes used in bioremediation. Metabolic and protein profiling, sequencing as well as the use of advanced bioinformatics resources are particularly used to unravel the different groups of microbes and the factors affecting them in bioremediation process ( Sharma et al., 2022b ). On the other hand, conventional and culture-dependent molecular methods are also used in the monitoring of microbial communities during bioremediation. These methods include the use of terminal-restriction fragment (T-RF) length polymorphism, amplified ribosomal DNA restriction analysis, temperature gradient gel electrophoresis, randomly amplified polymorphic DNA analysis, length heterogeneity polymerase chain reaction, amplified fragment length polymorphisms, denaturing gradient gel electrophoresis, length heterogeneity polymerase chain reaction, automated ribosomal intergenic spacer analysis and single strand conformation polymorphism ( Bharagava et al., 2019 ).

Moreover, omics approaches such as transcriptomics, proteomics and metagenomics have greatly contributed in this field. Metagenomics involve the extraction of genomic DNA from all forms of life residing in a sample. Thereafter, the DNA will be fragmented, cloned, transformed and screened in the metagenome library ( Bharagava et al., 2019 ). The approaches to metagenomics include metabolomics, metatranscriptomics, fluxomics and metabolomics. Metatranscriptomics involve the use of metagenomic mRNA which unravel the function and expression of microbes present in a sample ( Mukherjee and Reddy, 2020 ). Metaproteomics involved the assessment of all the protein samples that comes from environmental samples ( Bargiela et al., 2015 ). Metabolomics is the identification and quantification of all the metabolites released into an environment ( Liu et al., 2022 ). Fluxomics refers to the different approaches used to study the rate of metabolic activities in a biological sample ( Kumar V. et al., 2022 ). More recently, the use of Next-Generation sequencing which is viewed as the most powerful technology for gene sequencing has become more popular ( Eisenhofer et al., 2019 ).

8 Other bioremediation metabolites produced by microbes

Microbes produce metabolites such as organic acids, biosurfactants and polymeric substances which are also used in bioremediation. Organic acids improve the bioavailability, mobility and solubility of metals; examples of organic acids include citric acids, malate and acetic acids ( Saha et al., 2021 ). Polymeric substances are beneficial in bioremediation by enhancing the phytostabilization of metals (through mobility), examples of polymeric substances include polyesters, polysaccharides and polyphosphates. Equally, biosurfactants which include viscosin, polymixin, glycoprotein and gramicidin help to solubilise, mobilise and increase the bioavailability of hydrophobic substrates ( Ojuederie and Babalola, 2017 ; Saha et al., 2021 ).

9 Recent advancements in microbial bioremediate

Lately, many improvements have been observed with the use of microbes as agents of bioremediation. Microbial glycoconjugates help to reduce the surface tension, increase the bioavailability, and create a solvent interface of organic pollutants. This helps to enhance the removal of the pollutants in the environment ( Bhatt et al., 2021b ). Atakpa et al. (2022) reported the use of microbial glycoconjugates from Scedosporium sp. and Acinetobacter sp. in the biodegradation of petroleum hydocarbons.

Microbial biofilms which consist of polysaccharides, extracellular DNAs and proteins are also lately used in the bioremediation of organic pollutants ( Sonawane et al., 2022 ). They are particularly used in the remediation of recalcitrant pollutants. The technology is presently being made better by improving on the quorum sensing, environmental factors and surface of adhesion ( Sonawane et al., 2022 ). In a research carried out by Andreasen et al. (2018) , it was revealed that Exiguobacterium profundum was able to significantly reduce the concentration of arsenic in synthetic wastewater after 48 hours of incubation.

Bioelectrochemical system is another emerging technology which combines the use of biological and electrochemical methods in the control of pollutants ( Ambaye et al., 2023 ). This technology helps to majorly remediate petroleum hydrocarbon pollutants and its efficiency depends mainly on the syntrophic and cooperative interactions between the members of the microbial groups involved ( Ambaye et al., 2023 ). Sharma et al. (2020) stated that Pseudomonas sp. , Ralstonia sp. , Rhodococcus sp., and Thauera sp. are capable of remediating phenanthrene from petroleum hydrocarbon polluted soils.

Nanotechnology is a thriving method of pollution control globally. Nanomaterials can be sourced from different sources which include the physical and chemical sources ( Shanmuganathan et al., 2019 ). The efficiency of nanoparticles as bioremediation agents is dependent on different factors such as the size, chemical nature, surface coating and shape of the nanoparticles ( Tan et al., 2018 ). Other factors such as the nature of the pollutants, type of media, temperature and the environmental pH affect the potency of nanoparticles in the bioremediation process ( Tan et al., 2018 ). For instance, carbon dots nanoparticles have recently gained attention in the remediation of environmental pollutants owing to their abundance, low toxicity and unique optical properties ( Long et al., 2021 ). It is therefore necessary to carry out further research to unravel technologies and mechanisms to improve the efficiency of the bioremediation process.

10 Future perspectives and conclusions

A number of research endeavours have been carried out on the use of microbial enzymes for bioremediation of waste materials; however, it is very important to improve the process to ensure a safer and more sustainable environment. It is imperative to intensify research to unravel novel microbes that can effectively and rapidly bioremediate different pollutants, especially from industrial sources. Perhaps the novel microbes and their enzymes may have the inherent ability to bioremediate pollutants better than the presently used ones. It is also very important to carry out more studies to innovate rapid detection methods to reveal the progress or help to confirm total biodegradation of pollutants in the environment. Similarly, microbes presently used in bioremediation can be genetically modified to produce more enzymes which will enhance their biodegrading ability. A combination of different microbial consortium other than a single microbial consortium would be a better approach to bioremediation, as this would bring about the presence of different organisms which utilizes different substrate, consequently increasing the rate of microbial biodegradation.

Often, microbes are majorly used to degrade organic substrates, leaving out the persistent inorganic pollutants. Hence, research should be intensified to discover microbes that are capable of degrading inorganic (synthetic) pollutants. In recent years, nuclear wastes generated from the research sectors, hospitals, fuel processing plants and nuclear reactors have remained a global source of pollution. Therefore, the use of microbes and microbial enzymes in the bioremediation of nuclear wastes should be seriously taken into consideration. Occasionally, microbes themselves serve as a source of pollution instead of remediating pollutants. An example of such can be found when microbial biostimulation which results in algal bloom is carried out Consequently, methods to prevent this should be devised to ensure a sustainable environment.

Furthermore, in nature (outside the laboratory), the degradation of different compounds occurs at a different temperature, while the survival of microbes in nature are also environment-specific (temperature). It is therefore essential to carry out more field research to determine the optimum temperature for the degradation of different compounds in nature. In addition, it is also essential to find a balance between the environmental temperature and the temperature for the survival of different microbes in the environment. This would help to prevent bioremediation failure when external microbes are to be recruited or introduced to an environment. As positive and effective microbes might be recruited in the bioremediation of pollutants, it is important to carry out follow-up research to understand their effects on the environment after bioremediation, as some organisms which are introduced to an environment might later constitute pollution to the environment through mutation and other means. Hence, there should be regulatory bodies which would monitor the potential risk associated with microbes in specific environments.

Finally, if enzymes or microbes are directly applied to the soil, they might die or lose their potency before the remediation process begins; therefore, their combination with other agents, such as the nanoparticle could enhance their activity. More awareness is needed on the adoption of microbial degradation, and this will help policymakers as well as the populace to utilize this method. Many people unaware of this procedure might use the available conventional method, which might not be as safe and effective as the microbial biodegradation.

Author contributions

MA and OB conceptualized, wrote, reviewed, and edited the manuscript. All authors contributed to the article and approved the submitted version.

This research was funded by the National Research Foundation, South Africa, grant number UID: 123634; 132595.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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Keywords: microbial bioremediation, bioaugmentation, biostimulation, siderophores, biosorption

Citation: Ayilara MS and Babalola OO (2023) Bioremediation of environmental wastes: the role of microorganisms. Front. Agron. 5:1183691. doi: 10.3389/fagro.2023.1183691

Received: 10 March 2023; Accepted: 18 May 2023; Published: 30 May 2023.

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*Correspondence: Olubukola O. Babalola, b2x1YnVrb2xhLmJhYmFsb2xhQG53dS5hYy56YQ==

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