bioremediation of heavy metals by bacteria research paper

REVIEW article

Microbial interventions in bioremediation of heavy metal contaminants in agroecosystem.

• 1 Cell and Molecular Biology Laboratory, Department of Zoology (DST-FIST Sponsored), Soban Singh Jeena University Campus, Almora, India
• 2 Department of Biotechnology, Sir J C Bose Technical Campus, Kumaun University, Bhimtal, India
• 3 Department of Zoology, Kumaun University, Nainital, India
• 4 Department of Agricultural and Biological Engineering, PurdueUniversity, West Lafayette, IN, United States

Soil naturally comprises heavy metals but due to the rapid industrialization and anthropogenic events such as uncontrolled use of agrochemicals their concentration is heightened up to a large extent across the world. Heavy metals are non-biodegradable and persistent in nature thereby disrupting the environment and causing huge health threats to humans. Exploiting microorganisms for the removal of heavy metal is a promising approach to combat these adverse consequences. The microbial remediation is very crucial to prevent the leaching of heavy metal or mobilization into the ecosystem, as well as to make heavy metal extraction simpler. In this scenario, technological breakthroughs in microbes-based heavy metals have pushed bioremediation as a promising alternative to standard approaches. So, to counteract the deleterious effects of these toxic metals, some microorganisms have evolved different mechanisms of detoxification. This review aims to scrutinize the routes that are responsible for the heavy metal(loid)s contamination of agricultural land, provides a vital assessment of microorganism bioremediation capability. We have summarized various processes of heavy metal bioremediation, such as biosorption, bioleaching, biomineralization, biotransformation, and intracellular accumulation, as well as the use of genetically modified microbes and immobilized microbial cells for heavy metal removal.

Introduction

Contamination of heavy metals (HMs) has widely spread all over the world and therefore is a primary matter of concern as it poses threat to animals, plants as well as humans and disturbs the environment. HMs, like other metals and metalloids, are present in the earth’s crust, however, the recalcitrant nature of HMs makes them resistant to degradation. Bioaccumulation of HMs and metalloids via different sources like air, water, causes them to infiltrate plants, animals, and humans, as well as the advancement of the food chain over time ( Briffa et al., 2020 ). Several natural and man-made processes could release these HMs into the environment ( Dembitsky and Rezanka, 2003 ). Due to the growing usage of agrochemicals and inorganic fertilizers, modern agricultural methods have resulted in agricultural pollution, resulting in the ecosystem and environmental destruction ( Malik et al., 2017 ). HMs are also introduced into agricultural systems through the use of sewage sludge and organic waste manure, industrial wastes, and wastewater irrigation ( Srivastava et al., 2016 ; Sharma et al., 2017 ) ( Figure 1 ). Extraction of HMs from their ores occurs during the processing of minerals and throughout this process, some portions are left out in the open and get relocated to different places due to flood and wind thus causing serious environmental hazards. The essential nourishment of food crops is the soil and therefore agrarian soil is of huge concern owing to its linkage with the production of food, which could affect the health of living organisms. Despite being part of the soil, HMs cause serious harm to the soil as well as plants in their concentrated form. Thus, they are considered to be hazardous ( Osmani et al., 2015 ). HMs are responsible for not only changing the composition of soil but also forming the basis of stress in the plants resulting in the failure of the crop. Biological molecules like lipids, nucleic acids, proteins, and enzymes get damaged due to the production of free radicals by the HMs thus increasing intracellularly the reactive oxygen species (ROS) levels thereby leading to oxidative stress. The failure in all of these biological substances creates several physiological issues, including, cell damage, DNA damage, and enzyme inhibition, all of which can lead to the plant’s death ( Wu et al., 2016 ). HM pollution in modern agriculture has become a severe challenge in most emerging and underdeveloped countries due to a variety of social-economical, scientific, and developmental difficulties. Discovering environmentally safe, long-term solutions to the HM contamination problem is a serious task. Currently, the use of microorganisms or functional biocatalysts in the remediation of soil contaminated with HMs entails the integration of genomes, transcriptomics, proteomics, signaling systems, and synthetic biology knowledge ( Hemmat-Jou et al., 2018 ). These strategies offer a new vista in biotechnology, allowing for the creation of a complex biological system to produce a better microbial system capable of combating HMs contamination ( Sayqal and Ahmed, 2021 ). HMs affect the soil microbiology and modify rhizospheric connections between plants and microorganisms, influencing soil characteristics, plant growth, vegetation type, and agricultural land production, among other things. Different microbial communities with specific metabolic capacities reside in the soil, e.g., organic substances are formed by certain microorganisms while interacting with toxic metals whereas some other assists in the formation of natural nanoparticles thus reducing HMs ( Wang and Chen, 2006 ). Owing to their high surface area to volume ratio, which is associated directly with their increased reactivity, nanotechnology-based materials have also been explored for HMs micro-remediation ( Vijayaraj et al., 2019 ). The approaches and successes of biotechnological applications for environmental protection, decontamination, and the elimination of HMs and metalloids have thus been covered in this study.

Figure 1. The primary sources and effects of heavy metal exposure at various trophic levels.

The advancement of biotechnological applications and strategies for environmental protection, detoxification, and the removal of HMs and metalloids are the subject of this review. The goal of this review is to compile a list of key findings on HM contamination in modern agriculture, as well as to sketch a probable research roadmap for the future. The review explored the depth information about the mechanism and impacts of the HMs in microbial systems.

Heavy Metal Pollution in Agroecosystem: Consequences and Plant Responses

Effect on soil health, fertility, and microbial dynamics.

Soil biology plays a vital part in maintaining healthy soil quality, which is crucial for sustainable agriculture. The anthropogenic activities are central in contaminating soil with HMs, e.g., industrial, mining, and agricultural operations as the s present in mining waste, sewage sludge, inorganic fertilizers, and pesticides, tend to disturb soil microbes by percolating into the soil environment ( Gupta et al., 2010 ; Tóth et al., 2016 ; Sharma et al., 2017 ). With rising amounts of HM pollution, microbial viability declines. Yuan et al. (2015) showed that microbial survivability was found to be negatively correlated with prolonged Pb exposure. According to de Quadros et al. (2016) , coal mining operations; result in a decrease in microbial biomass, abundance, and variability. Nayak et al. (2015) reported that up to 40 and 100% fly ash amendments resulted in better microbial population dynamics with increased concentrations of Zn, Fe, Cu, Mn, Cd, and Cr in agricultural soils. Total microbial activity, as determined by the fluoresceindiacetate (FDA) test, and denitrifiers, on the contrary, exhibited an increasing tendency of up to 40% fly ash addition. The application of fly ash, on the other hand, reduced the activity of both acid and alkaline phosphatase. Various types of HM toxicity and their harmful effects on soil, plants, and humans are presented in Table 1 .

Table 1. Various types of heavy metal toxicity and their harmful effects on soil, plants, and humans.

Effect on Soil Microbial Functions and Processes

Due to HM toxicity, litter breakdown is slowed, resulting in an uneven litter deposit on the soil ( Illmer and Schinner, 1991 ; Giller et al., 1998 ; Marschner and Kalbitz, 2003 ). Kozlov and Zvereva (2015) investigated the breakdown rate of mountain birch ( Betula pubescens ssp. czerepanovii ) leaves in a significantly contaminated industrial setting close to the nickel-copper smelter in Monchegorsk. During 2 years of exposure, there was a substantial reduction of 49% in the relative weight of native leaves compared to the loss observed in the unpolluted forest. Furthermore, anthropogenic HM contamination has been found in a number of studies to have a negative impact on stream litter decomposition ( Carlisle and Clements, 2005 ; Hogsden and Harding, 2012 ; Ferreira et al., 2016 ). In both ecological toxicology and ecological tracking investigations, the rate of soil organic carbon mineralization has been routinely utilized as a test for metal toxicity ( Giller et al., 1998 ). Carbon mineralization may be measured using the soil respiration rate. A negative association was found between soil microbial respiration and HM concentration by Nwuche and Ugoji (2008) . From an average rate of 2.51–2.56 g of C/g at the start of the trial, the rate of soil microbial respiration was lowered to 0.98, 1.08, and 1.61 g of C/g in the Cu: Zn, Cu, and Zn treated soils, respectively. Because of differences in the experimental designs, fluctuations in soil characteristics, and substrate concentrations, HM exposure can either stimulate or impede N-mineralization. HM pollution disrupts nitrogen transformation pathways, which ultimately affects N-mineralization ( Dai et al., 2004 ; Vásquez-Murrieta et al., 2006 ; Hamsa et al., 2017 ). HM pollution has a similar impact on both N mineralization as well as nitrification i.e., both processes tend to decrease with an increasing amount of HM pollutants ( deCatanzaro and Hutchinson, 1985 ). Furthermore, nitrification is more susceptible to HM contamination than N mineralization ( Rother et al., 1982 ; Bewley and Stotzky, 1983 ).

Impact on Soil Enzymes

Metal composition, pH of the soil, organic matter, and clay content are important factors regulating the biological availability of metals in the soil. HMs affect soil enzymatic activity such as alkaline phosphatase, arylsulfatase, β-glucosidase, cellulase, dehydrogenase, invertase, protease, and urease ( Oliveira and Pampulha, 2006 ; Burges et al., 2015 ; Xian et al., 2015 ). Pan and Yu (2011) reported that HMs (Cd or/and Pb) reduce the activity of soil enzymes such as acid phosphatase, dehydrogenase, and urease, as well as the soil microbial community. Some researchers investigated the combined impact of HMs and soil characteristics on soil functions and concluded that arylsulfatase is the most sensitive soil enzyme that might be utilized as a marker of soil toxicity ( Xian et al., 2015 ).

Heavy Metals Responses in Plant System

Heavy metal contamination is a modern ecological issue that pollutes air, water, and soil. This not only results in significant crop yield losses but also raises health risks. In order to mitigate the damage caused by HM contamination, the antioxidative machinery of plants gets triggered.

Oxidative Stress and Reactive Oxygen Species

“Reactive oxygen species (ROS)” are reactive chemical species produced from molecular oxygen. Various diverse ROS are present momentarily among all aerobes which include: (a) oxygen-derived non-radicals viz. singlet oxygen ( 1/2 O 2 ), organic hydroperoxide (ROOH), hydrogen peroxide (H 2 O 2 ); and (b) oxygen-derived free radicals viz. superoxide anion (O 2 – ), alkoxyl (RO⋅) radicals, peroxyl (RO 2 ⋅), and hydroxyl (HO⋅) ( Circu and Aw, 2010 ; Shahid et al., 2014 ; Tamás et al., 2017 ). Plants tend to produce more ROS, after exposure to HMs as they can disrupt the electron transport chain of the mitochondrial and chloroplast membrane. The increased load of ROS interrupts the redox balance of the cell by causing plasma membrane damage and ion leakage ( Dingjan et al., 2016 ; Anjum et al., 2017 ), lipid peroxidation, and the disintegration of cellular macromolecules ( Carrasco-Gil et al., 2012 ; Chen et al., 2012 ; Venkatachalam et al., 2017 ). The increased amount of Cr in two maize genotypes reduced the content of soluble protein and elevated the level of phenol, proline, and other soluble sugars ( Anjum et al., 2017 ).

Genotoxicity

The pathways regulating metal-induced genotoxicity are intricate and are understudied ( Cuypers et al., 2011 ). However, it is clear that HM-induced genotoxicity/DNA damage happens indirectly via the generation of ROS during oxidative stress ( Barbosa et al., 2010 ; Shahid et al., 2014 ; Aslam et al., 2017 ). HM-induced nucleic acid impairments have previously been identified in plants such as Helianthus annuus ( Chakravarty and Srivastava, 1992 ), Vicia faba ( Pourrut et al., 2011 ; Arya et al., 2013 ; Arya and Mukherjee, 2014 ), Solanum tuberosum , and Nicotiana tabacum ( Gichner et al., 2006 ), and Allium cepa ( Arya et al., 2013 ; Arya and Mukherjee, 2014 ; Qin et al., 2015 ). The oxidation state of HM, its amount, and duration of exposure greatly affects the genotoxic response of any plant ( Aslam et al., 2017 ). The extremely reactive species among ROS is the hydroxyl radical (OH⋅), which can react to and damage all of the DNA molecule’s components ( Jones et al., 2011 ). When ROS react with DNA, it can cause deletion, and modification of nitrogenous bases, breakage of strands, damage to cross-links, and generation of nucleotide dimmers ( Gastaldo et al., 2008 ). When Pb and Cd react with DNA, Yang et al. (1999) detected the formation of 8-hydroxydeoxyguanosine (8-OHdG) adducts, which resulted in the breaking of the strand. Further, Hirata et al. (2011) reported Cr and As-triggered translesion DNA synthesis as a consequence of 8-OHdG production. Several recent studies were made on the genotoxic effects of copper and lead ( Qin et al., 2015 ; Silva et al., 2017 ; Venkatachalam et al., 2017 ).

Interference With Signaling Pathways

Deregulation of signaling pathways mediated by HM interactions is the main cause behind HM toxicity by influencing G-proteins, growth factor receptors, and receptor tyrosine kinases ( Harris and Shi, 2003 ). HMs also boost H 2 O 2 production in plants by increasing the synthesis of salicylic acid (SA), jasmonic acid (JA), and ethylene (ET), which interferes with the cell signaling mechanism ( Maksymiec, 2007 ; Schellingen et al., 2014 ; van de Poel et al., 2015 ). Plants exposed to As, have higher levels of JA, which stimulates the expression of several signaling and stress-response genes such as MAPK, CDC25, and genes regulating glutathione metabolism ( Thapa et al., 2012 ; Islam et al., 2015 ).

Physiological and Biochemical Response

The anti-oxidative enzymatic machinery of plants such as ascorbate peroxidase (APX), catalase (CAT), glutathione (GSH), glutathione reductase (GR), guaiacol peroxidase (GPX), peroxidase (POX), and superoxide dismutase (SOD) plays a critical role in neutralizing extra ROS ( Zhang and Klessig, 2001 ; Venkatachalam et al., 2017 ). Increased MDA generation due to enhanced ROS in the cell was observed when two mangrove plants were exposed to HMs ( Zhang and Gu, 2007 ). Similarly, superoxide dismutase (SOD) level was dramatically increased in leaves and roots at low metal concentrations, but dropped drastically at greater concentrations, suggesting a reduction in SOD scavenging ability. Abelmoschus esculentus plant grown on sewage sludge reflected an initial increase in chlorophyll content but fall sharply in later stages. The apparent decrease in chlorophyll content might be due to the accumulation of HMs in plants at later stages ( Singh and Agrawal, 2008 ). Similar findings were made in Vigna radiata ( Singh and Agrawal, 2010 ) and Oryza sativa ( Singh and Agrawal, 2010 ).

Microbial Resistance to Heavy Metals and Their Mechanisms

During stress situations developed by HMs, microorganisms either dies of the toxicity caused by the metal or thrive the situation by evolving mechanism of resistance against metals. For the selection of potent bioremediation agents, microorganisms should develop the mechanism of resistance against the toxicity of metals. Different resistance mechanisms developed by microorganisms like Extracellular barriers, extracellular and intracellular sequestration, active transport of metal ions, and enzymatic detoxification are discussed below ( Figure 2 ). Barriers like cell walls, plasma membrane, and other structures present at the surface like EPS, biofilms restrict the passage of HMs into the cells of bacteria. Microbes’ cell surfaces have a variety of characteristics that prevent metal ions from entering by adsorbing them on their surface and functioning as barriers. E.g., a study by Kumar et al. (2014) showed that isolates of fungi and bacteria can cause biosorption of HMs like copper, lead, and chromium. Tolerance against numerous HMs like copper, zinc, iron, nickel, lead, and cadmium was shown by Cellulosimicrobium sp. Chemisorption sites were involved in this resistance mechanism ( Bhati et al., 2019 ). The Biofilms produced by microbes are made up of extracellular polymers that are capable of accumulating metal ions and therefore protect the cells present inside them. The tolerance against lead, zinc, and copper ions has been displayed by the biofilm of Pseudomonas aeruginosa ( Teitzel and Parsek, 2003 ). The efficiency to eliminate metal was enhanced from 91.71 to 95.35% by the biofilm of Rhodotorula mucilaginosa ( Grujić et al., 2017 ). In addition to biofilms and cell walls, EPS has also been shown to be a barrier against metals, e.g., Adsorption of lead ions was reported in P. aeruginosa , Acinetobacter junii L. Pb1, and Azotobacter chroococcum XU1 ( Bramhachari et al., 2007 ; Rasulov et al., 2013 ; Kushwaha et al., 2017 ).

Figure 2. Microbe-mediated environmental remediation of heavy metals.

Numerous proteins and metabolic products are found in the cell membrane of the microbes that are capable of making complex structures (chelation) with the metal ions. Extracellular sequestration can be defined as the complexation of metal ions as insoluble compounds or metal ions accumulation by the components of the cell in the periplasm. Copper-inducible proteins CopA, CopB (periplasmic proteins), and CopC (outer membrane protein) are produced by copper-resistant Pseudomonas syringae strains that are responsible for the binding of microbial colonies and copper ions. Zinc ions can pass from the cytoplasm and get accumulated into the periplasm of the Synechocystis PCC 6803 strain via the efflux mechanism ( Thelwell et al., 1998 ). Hazardous metals can be reduced by iron and sulfur-reducing bacteria like Desulfuromonas spp. and Geobacter spp. into less or non-hazardous metals. An obligate anaerobe, G. metallireducens , can reduce manganese (Mn) from poisonous Mn (IV) to Mn (II) and uranium (U) from toxic U(VI) to U(II) (IV) ( Gavrilescu, 2004 ). In intracellular sequestration, metal ions are complexed by distinct compounds in the cell cytoplasm. The interaction of metals with the ligands presents in the surface, followed by sluggish transport into the cell, can result in a high concentration of metals within the cells of microorganisms. The ability to accumulate metals intracellularly by bacterial cells has been used in a variety of applications, most notably in waste treatment. With the help of low molecular weight proteins that were rich in cysteine, a cadmium-tolerant Pseudomonas putida strain was able to sequester copper, cadmium, and zinc ions intracellularly ( Higham et al., 1986 ). In Rhizobium leguminosarum cells, glutathione was also found to be involved in the sequestration of cadmium ions intracellularly ( Lima et al., 2006 ). Lipids, chitin, mineral ions, nitrogen-bearing polysaccharide, polyphosphates, and proteins make up the firm cell wall of fungi. The accumulation of metals by numerous fungi into their spores and mycelium helps in decontaminating metal ions by energy uptake, intracellular and extracellular precipitation, and valence exchange. Another strategy to protect against HM stress is to transport HM ions out from the intracellular environment, which can happen through efflux mechanisms that can effectively regulate intracellular HM ion concentrations ( Remenar et al., 2018 ). Efflux systems have been discovered in a variety of microbes, particularly those isolated from metal contaminated surroundings. Metal exporting proteins, such as ABC transporters, P-type efflux ATPase, cation diffusion facilitator, and proton-cation antiporters are widely distributed in the cell membrane to achieve HM ion efflux. For the export of Cu (II), Cd (II), and Zn (II), Gram-positive bacteria utilize P-type efflux ATPase. With the help of ATPase, an exporting protein on the cell membrane regulates arsenite outflow ( Yang et al., 2012 ; Soto et al., 2019 ). ABC transporters which also called traffic ATPases can assist microorganisms to survive the stress caused due to HMs by mediating membrane translocation of HM ions ( Al-Gheethi et al., 2015 ; Lerebours et al., 2016 ; Zammit et al., 2016 ).

The resistance to HMs ions in microbes is also contributed by the enzymes that biologically transform or chemically modify the HM ions from highly hazardous form to less toxic form ( Liu et al., 2017 ). HM ions’ toxicity can be effectively reduced by changing their redox state via reduction or oxidation reactions ( Giovanella et al., 2016 ). Detoxification enzymes can influence this defensive mechanism, which is also controlled by microbe resistance genes. Through mercuric ion reductase, bacteria like Bacillus sp. display resistance to mercury ions ( Noroozi et al., 2017 ). Mercuric reductase transforms the mercuric ion into metallic mercury, which is then discharged into the environment via the cell membrane ( Zhang et al., 2012 ). To reduce toxicity, bacteria such as Micrococcus sp. and Acinetobacter sp. can oxidize hazardous as (III) into less soluble and non-toxic As (V) ( Nagvenkar and Ramaiah, 2010 ).

Microbial Mechanism Involved in Heavy Metal Bioremediation

For the elimination of HMs from the polluted sites, bioremediation methods are employed ( Pratush et al., 2018 ). Usually, these methods involve the absorption/adsorption of toxic metallic ions, and this alleviates the related side effects ( Njoku et al., 2020 ). Different natural resources like wood bark/dust, coconut husk/shells, agro wastes, microorganisms, seaweeds, seeds, discarded coffee beans, and aquatic plants, etc. are being used constantly to reduce the number of HM ions from the place of their origin, in which microbes (algae, fungi, bacteria, yeasts, etc.) play a considerable role ( Mudila et al., 2019 ). Microorganisms change the HMs’ ionic state that influences the solubility, bioavailability, and movement in the soil as well as in the aquatic surroundings ( Ayangbenro and Babalola, 2017 ). Mobilization or immobilization of HMs aids microbial remediation, which is then proceeded by oxidation-reduction, chelation, modification of the metallic complex, and biomethylation ( Pratush et al., 2018 ). The enzymatic catalysis by microbes solubilizes the metals with higher oxidation state to lower oxidation state, for instance, Thiobacillus ferrooxidans and T . thiooxidans are responsible for the enzymatic oxidation of Uranium ( Cumberland et al., 2016 ). The isolation of microorganisms responsible for the degradation of HMs could occur from aerobic as well as anaerobic locations. However, in comparison to anaerobic microorganisms, aerobic microbes are more willing for bioremediation ( Azubuike et al., 2016 ). Microorganisms carry out the transportation of HMs utilizing membrane-linked transport mechanisms and transform them into non-hazardous forms ( Igiri et al., 2018 ). Microorganisms use processes like biosorption, bioaccumulation, biotransformation, and bioleaching to stay alive in a metal-polluted environment ( Figure 2 and Table 2 ). These techniques have been used in clean-up processes ( Gadd, 2000 ; Lin and Lin, 2005 ).

Table 2. Microbe-mediated remediation and resistance mechanism of heavy metals.

Bioaccumulation and Biosorption

Both bioaccumulation and biosorption are the processes utilizing which microbes or biomass gets bound to the HMs and pollutants from the surroundings and concentrates them ( Joutey et al., 2015 ). However, the working manner of the processes differs. Biosorption is a process in which microorganisms use their cellular structure to capture HM ions, which they then sorb onto the cell wall’s binding sites ( Malik, 2004 ). This is a passive uptake process and does not depend upon the metabolic cycle. Two common methods for the bioremediation of HMs are adsorption and absorption onto the cell surface of microbes. Adsorption differs from absorption in that it involves the dissolution or permeation of a fluid (the absorbate) by a liquid or solid (the absorbent) ( Jovancicevic et al., 1986 ). Adsorption, on the other hand, is a surface occurrence, whereas absorption affects the full volume of the substance. Various living creatures have been shown to be possible bio sorbents e.g., bacteria like Magnetospirillum gryphiswaldense, Bacillus subtilis , algae-like marine microalgae, and Chaetomorphalinum , fungi like Rhizopus arrhizus and yeast-like Saccharomyces cerevisiae ( Romera et al., 2006 ; Wang and Chen, 2009 ; Zhou et al., 2012 ). Bacteria, on the other hand, are regarded as the most exceptional biosorbents among all other creatures due to their high surface-to-volume ratios and numerous chemosorption active sites in their cell wall, such as teichoic acid ( Beveridge, 1989 ). Dead bacterial strains have also been considered as promising biosorbents, with biosorption abilities that exceed those of living cells of the same strain. 13–20% increased capacity for the biosorption of chromium ions was shown by dead Bacillus sphaericus as compared to the cell of its living strain ( Velásquez and Dussan, 2009 ). However, unlike biosorption, bioaccumulation by microbes is metabolically active and relies upon the import-storage system. In this system, HM ions are transported through the lipid bilayer of the cell membrane into the intracellular spaces or cytoplasm with the help of transporter proteins. This is known as active uptake or bioaccumulation. Endocytosis, ion channels, carrier-mediated transport, complex permeation, and lipid permeation are all involved in HM bioaccumulation in the bacterial membrane ( Ahemad, 2012 ; Geva et al., 2016 ; Shahpiri and Mohammadzadeh, 2018 ). Bioaccumulation studies of various metals like lead, nickel, silver, mercury, and cadmium have been reported by Ahemad (2012) . The study of cadmium by Rani and Goel (2009) discovered periplasmic and intracellular metal accumulation by P. putida 62 BN, and it was performed using transmission electron microscopy. The growing cells of Bacillus cereus M116 were shown to accumulate about 20% nickel (II) intracellularly, as reported by Naskar et al. (2020) . Lead and chromium accumulation by Aspergillus niger and Monodictys pelagic was reported by Sher and Rehman (2019) . In the process of bioleaching, metal oxides and sulfides from ores deposits and secondary wastes are solubilized by different microorganisms like fungi and bacteria ( Mishra et al., 2005 ; Jafari et al., 2019 ). Following solubilization, purification is achieved with the help of appropriate methods like ion exchange, selective precipitation, adsorption, and membrane separation ( Rohwerder et al., 2003 ).

Bioleaching

Bioleaching is performed by an extensive range of microbes and among them, acidophiles are the prominent ones. Acidophiles are chemolithotrophs that oxidize Fe (II) to Fe (III) and/or reduce sulfur to sulfuric acid and flourish in low pH environments, particularly 2.0 or below. Sulfuric acid produces ferric ions and protons, which solubilize metal sulfides and oxides from ores ( Srichandan et al., 2014 ), aiding extraction of metal by segregating metals in the solid phase from the more water-soluble phase. Bioleaching, which uses microorganisms as reduction agents, can also be used to extract and recover heavy metals ( Wang and Zhao, 2009 ). The ability of microorganisms to convert the solid chemical within contaminated soil into a soluble substance that can be removed and recovered determines the efficacy of the recovery process. Due to metal resources being non–renewable, recovering metal from industrial waste water may be a viable option for ensuring heavy metal supply ( Atkinson et al., 1998 ). Bioremediation has been offered by a number of researchers as a way to recover raw materials from effluent ( Pollmann et al., 2006 ; Gadd, 2010 ). Using an Annona squamosa -based absorbent with 0.1 M HCl, Cd(II) recovery up to 98.7% was achieved ( Isaac and Sivakumar, 2013 ). Using Pseudomonas aeruginosa biomass with 0.1 M HCl, a Cd(II) recovery up to 82% was achieved. Using volcanic rock matrix-immobilized P. putida cells with surface-displayed cyanobacterial metallothioneins at pH 2.35 ( Ni et al., 2012 ), 100% Cu(II) recovery was reported. Using activated sludge at pH 1.0 resulted in a 100% recovery of Cu(II) ( Hammaini et al., 2007 ). The introduction of an indigenous strain Enterobacter sp. J1 resulted in a Cu and Pb recovery of over 90% at pH 2 ( Lu et al., 2006 ).

Biotransformation

Biotransformation is a process in which structurally a chemical compound is altered, thereby relatively a more polar molecular is synthesized ( Asha and Vidyavathi, 2009 ; Pervaiz et al., 2013 ). In other words, this contact of metal and microorganisms causes toxic metals and organic compounds to get altered to a comparatively less hazardous form. The development of this mechanism in the microorganisms causes them to acclimatize the environmental changes. Microbial transformations can be attained through the production of new carbon bonds, isomerization, introducing functional groups, oxidation, reduction, condensation, hydrolysis, methylation, and demethylation. Transformation of metals by application of microbes has been reported. Micrococcus sp. and Acinetobacter sp. oxidize hazardous As (III) into less soluble and non-toxic As(III) and reduce its toxicity ( Nagvenkar and Ramaiah, 2010 ). Thatoi et al. (2014) reported that Cr (VI)-tolerant Bacillus sp. SFC 500-1E through NADH-dependent reductase has been shown to lessen the hazardous Cr (VI) to less toxic Cr (III).

Influence of Environmental Change on the Remediation of Heavy Metal Contaminants

The pH is important for microbial biosorption, and the optimal pH varies depending on the microbe. Firstly, pH influences the enzymatic activity in bacteria, altering the rate of HM microbial metabolism ( Morton-Bermea et al., 2002 ). Secondly, pH alters the microorganism’s surface charge, affecting its ability to adsorb HM ions ( Galiulin and Galiulina, 2008 ). Besides this, pH has an impact on the hydration and movement of a variety of metal ions in the soil ( Dermont et al., 2008 ). Both Rodríguez-Tirado et al. (2012) and Wierzba (2015) found that the rate of HMs removal by microbe upsurges with an increase in pH across a certain range, but after the pH climbs to a specific level, the elimination rate begins to decline. According to a study the ideal pH range for most bacteria, is 5.5–6.5, however there are exceptions ( Wang et al., 2001 ). For instance, Bacillus jeotgali thrives at a pH of 7. This could be because as the pH rises over a certain point, some metal ions form hydroxide precipitates, which are less prone to microbial adsorption ( Hu et al., 2010 ; Rodríguez-Tirado et al., 2012 ). Furthermore, the optimal pH for aerobic microbes and anaerobic microorganisms may differ.

The rate of absorption of HM is mostly influenced by ambient temperature, which impacts the growth and multiplication of microorganisms ( Fang et al., 2011 ). Various bacteria have different optimal temperatures ( Acar and Malkoc, 2004 ) for example, Acidianus brierleyi and Sulfolobussolfa-tataricus are very thermophilic bacteria, while, Thiobacillus acidophilus , Thiobacillus tepidarius , and Thiobacillus ferrooxidans are medium temperature bacteria.

When it comes to understanding substrate species, there are three things to keep in mind: HM ions, soil additives, and the type of soil. HM adsorption characteristics on different soils might be quite varied. According to a study, beach tidal soil (Freundlich adsorption constant K = 93.79) has a larger adsorption capacity than black soil ( K = 16.41), which is higher than yellow mud ( K = 1.17), and that the mean desorption rate of soil is Lithic Ochri-Aquic Cambosols in ascending order (0.67%), Fe-accumulic Gleyic Stagnic Anthrosols (3.62%), and Endogleyic Fe-accumulic Stagnic Anthrosols (35.85%) ( Chen et al., 1997 ). Clearly, soil’s adsorption rate and retention of HM ions result in poor mobility of HM ion, making microbial adsorption difficult to achieve ( Hu et al., 2010 ). HM ion species influence HM elimination by changing microbial generation time. The generation period of Thiobacillus ferrooxidans on sulfur as a substrate is about 10–25 h, which is significantly longer than the 6.5–15 h generation time on Fe. Moreover, the existence of metal ions in the soil affects microbial enrichment ( Kapoor and Viraraghavan, 1997 ). Individual bioavailability of Pb2+, Cd2+, and Zn2+ in the soil is often more than that of several metal ions, according to Park et al. (2016) . The adsorption of Cd2+ alone is 11.2 mg/g. Its adsorption is reduced to 3.15 mg/g in the presence of Zn2+ and Pb2+, with similar results for Zn2+ and Pb2+, displaying the reduction from 19.5 and 2.25 to 8.08 and 0.915 mg/g, respectively. Soil additions can considerably boost microbial removal of HMs, and the concentration of additives can have varied impacts on HM ion leaching rates. Tyagi et al. (2014) found that adding 20 g/L FeSO4.7H2O to a solution increased the leaching rate of Zn and Cu by 2 and 1.9 times, respectively, but not when the concentration was larger than 20 g/L. The adsorption rate of microorganisms is also affected by the concentration of HM ions. To estimate the quantification of accumulative properties of a bio-sorbent, adequate assessment is required in general ( Cervantes et al., 2001 ). The Langmuir model, whose parameters are interpretable and primarily explains the adsorption of a single-layer surface, is one of the most commonly used equations to describe the features and another Freundlich model, is mostly employed to the adsorption equilibrium of the adsorption surface equation ( Febrianto et al., 2009 ). Despite the fact that the Freundlich model is simpler, it grows unbounded, hence the Langmuir model has been more extensively employed than the Freundlich model until recently. The Langmuir model was utilized by some researchers to investigate the influence of HM concentration ( Ehrlich, 1997 ; Brunetti et al., 2012 ). They discovered that depending on the microorganisms and HM ions investigated, the concentrations of HM ions with the highest adsorption rates change. Though, the trend, which is consistent across all examples, implies that adsorption increases to a certain point and then remains constant as HM ion concentrations rise.

Modern Approaches in Microbe-Intervened Biotechnologies

Rhizoremediation: the phyto-microbial remediation system.

Rhizoremediation combines two methods for cleansing polluted substrates: phytoremediation and bioaugmentation. Rhizoremediation is the process of using microorganisms found in the rhizosphere of plants that are involved in the phytoremediation process. Application of plants and plant growth-promoting bacteria (PGPB) is being assessed as an effective and environmentally acceptable way for soil renewal and HMs elimination, among the several integrated techniques ( Ali et al., 2013 ; Sati et al., 2022 ). Many microorganisms in the rhizosphere, such as mycorrhizal fungi and other rhizospheric organisms, can help plants absorb or adsorb HMs ( Bojórquez et al., 2016 ). Joner and Leyval (1997) found that mycorrhizal plants uptake 90, 127, and 131% more Cd than non-mycorrhizal plants, when the concentration of Cd 2+ in the soil is 1, 10, and 100 mg/kg, respectively. Bissonnette et al. (2010) displayed that mycorrhiza inoculation improves the ability to absorb Cu2+, Cd2+, and Zn2+. Mycorrhizal fungi possess mycelia that grow into the soil, thereby increasing the surface area of plant roots ( Trellu et al., 2016 ). For metal extraction with plants, PGPR including Azospirillum, Alcaligenes, Agrobacterium, Arthrobacter, Burkholderia, Bacillus, Pseudomonas, Rhizobium , and Serratia , are commonly utilized ( Carlot et al., 2002 ; Glick, 2003 ). Metal transformation, immobilization, chelation, or solubilization is aided by the production of exopolysaccharides by PGPB, like oxidases, reductases, siderophores, and organic acids which promotes phytoremediation of HMs. PGPB reduces the pH of the soil by producing organic acids, which aids in the removal of HM ions. Metal resistant siderophore-producing bacteria found near the rhizosphere supply nutrients to the plants namely iron, perhaps reducing the negative consequences of metal contamination ( Dimkpa et al., 2008 ; Sinha and Mukherjee, 2008 ). Siderophore is also responsible for the formation of stable complexes with radionuclides and metals concerning environment like Cd, Ga, Al, Cu, Zn, In, and Pb ( Neubauer et al., 2000 ; Rajkumar et al., 2010 ). The synergistic effects of bioaugmentation and phytoremediation leading to rhizoremediation may overcome the difficulties that arise when both processes are employed distinctly. Moreover, the remediation of HM with the help of higher plants has also been reported. Wang et al. (2021) also found that planting Salix in Cd-polluted soil improved the diversity of beneficial microbes, such as the bacteria genera Arthrobacter and Bacillus. Anaeromyxobacter, Novosphingobium, Niabella, Niastella, Flavobacterium, Thermomonas, Lysobacter, Pedomicrobium, Solitalea, Devosia, Flavisolibacter, Mesorhizobium, Nitrospira, Rmlibacter , and Rubrivivax. Phyllobacterium and mycorrhizal genera of fungi include Amanita, Cryptococcus, Conocytes, Actinomucor, Ramicandelaber, Spizellomyces, Xylaria, Rhodotorula, Umbilicaria, Sporobolomyces, Tilletiopsis, Claroideoglomus , and Cirrenaliain plant rhizosphere.

Genetically Engineered Organisms and Modern Molecular Biology

Bioremediation using microorganisms can degrade and dissipate chemicals of complex substances, making it a long-term solution for reducing HMs contamination in soil ( Mosa et al., 2016 ; Bhatt et al., 2020a , b ). Recent advances in genetic engineering, as well as the adequacy of genetically engineered microorganisms/biocatalysts for the restoration of the environment, have shown that they are more capable than natural microbes, particularly for the removal of persistent compounds under natural environments ( de Lorenzo, 2009 ; Bhatt et al., 2020c ). By the application of various genetic and metabolic engineering approaches, the genetic material of microbes is modified, and engineered microorganisms are produced which are more efficient thus resulting in enhanced bioremediation. Single-gene editing, pathway construction, and change of existing gene sequences i.e., both coding as well as controlling sequences are included in the aspects of engineering, with a focus on the modification of rate-limiting stages of the metabolic processes ( Diep et al., 2018 ). HMs such as Fe, Cd, As, Cu, Hg, and Ni can now be eliminated with the help of engineered bacteria ( D’Souza, 2001 ; Verma and Singh, 2005 ; Azad et al., 2014 ). The rate of degradation, on the other hand, is determined by the catalytic efficiency of enzymes present in the cells or those stimulated to a specific substrate ( Kang, 2014 ). Using recombinant DNA technology, foreign genes from another creature of the same or other species are put into the genome of genetically engineered microorganisms (GEMs). The utilization of genetically modified Pseudomonas putida and Escherichia coli strain M109 harboring the merA gene to successfully remove Hg from polluted soils and sediments has been reported ( Chen and Wilson, 1997 ; Barkay et al., 2003 ; Deckwer et al., 2004 ). Azad et al. (2014) provided a thorough evaluation of the application of genetically modified bacteria and plants in the bioremediation of HMs and other organic pollutant-contaminated environments. According to a study, the addition of the mer operon from Escherichia coli , which codes for the reduction of Hg2+, into the genetically modified bacterium Deinococcus geothemalis provides the ability to microorganism to lessen the Hg pollution at high temperatures by mer genes ( Dixit et al., 2015 ). Cupriavidus metallidurans strain MSR33, which was genetically engineered with a pTP6 plasmid that provided genes merB and merG which regulate the biodegradation of Hg as well as the production of merB and merA, i.e., organomercurial lyase protein and mercuric reductase, was able to reduce Hg contamination from polluted sites ( Rojas et al., 2011 ; Dixit et al., 2015 ). The insertion of novel genes into Pseudomonas cultures using the pMR68 plasmid has also resulted in Hg resistance ( Sone et al., 2013 ). Specific genes in n-alkane-degrading microbes, such as alkB, alkB1, alkB2, alkM, aromatic hydrocarbons: xylE, and polycyclic aromatic hydrocarbons: nidA, ndoB, are frequently found on plasmids that allow horizontal gene transfer and are employed as markers to identify microbial biodegradation ( Wolejko et al., 2016 ). Microbial membrane transporters can be genetically modified to improve the bioremediation of HMs in the environment. Transporters and binding mechanisms play crucial roles in this context of HMs remediation ( Manoj et al., 2020 ). Channels, secondary carriers, and primary active transporters are the three principal types of transporters that are usually emphasized. Their location is in the inner lipid membrane such as Fps, Mer T/P, and GlpF in channel transporters; Hxt7, NixA, and Pho84 in secondary carriers; and cdtB/Ip_3327, MntA, TcHMA3, and CopA in primary active transporters. Some of them, such as the porin channels transporters, may also be found in the outer lipid membrane ( Jain et al., 2011 ). As soon as HMs comes inside the cell, numerous phytochelatins, metallothioneins, and polyphosphates work together for the sequestration of the HMs and changing microorganisms’ HM import-storage systems could boost their ability to extract HMs from water and soil ( Diep et al., 2018 ). Thus, in the fight against harmful compounds in the environment, the use of GEMs to speed up the restoration process is crucial. For the successful implementation of GEMs for bioremediation in adverse environmental conditions, the preservation of recombinant bacterial population in the soil is essential, with appropriate environmental conditions prepared and the recombinant bacteria should be capable to endure antagonism from native bacterial species ( Dixit et al., 2015 ). Consequently, further novel molecular approaches for the screening and isolation of microbes for HM bioremediation should be investigated. Multi-omics comprising genomics, metagenomics, metabolomics, proteomics and transcriptomics, and computational biology techniques have been successfully employed in gene mining that supports system biology research of microorganisms at the genetic level concerning bioremediation of HMs ( Subashchandrabose et al., 2018 ; Pande et al., 2020 ; Sayqal and Ahmed, 2021 ). Novel genes implicated in the biodegradation processes of several HM contaminants have been discovered because of high-throughput and next-generation sequencing. New technologies involve gene-editing tools like CRISPR-Cas which possesses the ability to enhance the process of bioremediation by engineering microorganisms with genes engaged in the degradation of, particularly recalcitrant substances. When compared to conventional low-throughput ZFNs and TALENs, CRISPR might be utilized to transmit a preferred set of instructions into the genome of microbe in a straightforward manner because it is a programmable, next-generation approach for high-throughput genetic manipulation ( Miglani, 2017 ). A CRISPR segment is likely for the bioremediation by the application of gRNA-guided dCas9 to control the expression of a gene. As a result, fusing transcription factors with dCas9 can either suppress boost or suppress RNA polymerase transcription, which can cause either upregulation or downregulation of the gene expression or a set of genes of interest. Although CRISPER-based approaches can be employed on a variety of mycobacteria and fungi, further applied research in the area of microbe-based removal of HMs from the environment is needed ( Shapiro et al., 2018 ). With the help of multi-omics, biotechnology has developed a large number of strains. The following are some examples Arthrobacter, Chlorella ( Gong et al., 2018 ), Stenotrophomonas maltophilia ( Cho et al., 2018 ), Rhodococcus wratislaviensis, Mycobacterium ( Gołêbiewski et al., 2014 ), Alcaligenes eutrophus, Pseudomonas putida ( Cycon and Piotrowska-Seget, 2016 ), Cyanobacterium synechocystis , Saccharomyces cerevisiae , Populus sp. ( Cai et al., 2019 ), Candida pelliculosa strain S-02, Streptomyces aureus strain HPS-0, Aspergillus niger ( Kumar et al., 2018 ), Sphingomonas sp., and Pseudomonas putida strain KT2440 ( Liu et al., 2019 ).

Nanotechnology in Microbial Bioremediation

With the application of chemical or biological methods, several types of nanoparticles have been effectively produced and studied for bioremediation of HMs, over the last decade ( Baragaño et al., 2020 ). The advantages of nano-biosorbents with an ultrafine arrangement and a great surface area include (1) enhancing chemical activity and capacity of adsorption, (2) boosting surface binding energy, and (3) lowering internal diffusion resistance ( Khati et al., 2017 ). As a result, nano-biosorbents could be used as a replacement for traditional biosorbents ( Abdi and Kazemi, 2015 ; Alviz-Gazitua et al., 2019 ). Latest advancements in the nanobiosorption model have resulted in a number of sophisticated ways that improve the complete efficiency of a conventional biosorption process while also ensuring its economic viability ( Devatha et al., 2018 ). Different functional groups, such as –NH 2 , –COOH, and –OH, are intrinsically present in nanoparticles, and tailoring the appropriate functional groups by activating physically/chemically or by modifying surface has proven to improve elimination of HMs. Bacterial strains can also produce nanoparticles that can aid in the bioremediation of HMs ( Arshad et al., 2019 ). Nanomaterials are combined with microbes to improve reduction of HMs, which makes them more effective as compared to their independent application. Factors in determining the interaction between nanomaterials and microbes include (1) the chemical properties of the nanomaterial, its particle size, coating characteristics, and shape, (2) the chemical properties of the nanomaterial, along with the shape, size of the particle, and its coating characteristics, (3) method of metabolism, (4) the nanomaterial’s crystalline phase, (5) the extent of contamination and, lastly (6) the resistance of nanomaterials to the hazardous contaminant and the prevalent ecological conditions. Microbial biostimulation, bioaccumulation, and biotransformation activities are enhanced by nanocomposites, which increase absorption, adsorption, and the number of chemical processes for the reduction of HMs ( Tan et al., 2018 ). Microbes are trapped within nanomaterials to create a nanocomposite; for example, immobilization of gram-negative Halomonas sp. within polyvinyl pyrrolidone-coated iron oxide nanoparticles was confirmed to eliminate Pb (II) and Cd (II) ( Cao et al., 2020 ). On the other hand, the microbe can function as a nanoparticle synthesizer, a method known as green synthesis. Though separating or recovering HMs from nanomaterials, is a time-consuming/laborious technique and hence magnetic nanoparticles have gained considerable attention in recent years, wherein surface amendment, coating of iron/iron oxides, and encapsulation focused for simple separation or retrieval of HMs.

Throughout the world, HM contamination causes severe environmental problems. In this review, several technical strategies i.e., microbe-based as well as hybrid have been discussed, that are currently being employed to mitigate HM contamination in soils and other contaminated surroundings. Because of the contribution in the regulation of biogeochemical cycles that influence climate, soil structure, and fertility, the environmental microbiome is thought to play a critical role. Microbe-mediated bioremediation should be given high attention from a practical standpoint since microbes have a variety of natural roles and mechanisms that considers them a great candidate for the clean-up of the polluted site, management of wastes, and sustainable agriculture. Although microbes are being employed to improve the effectiveness of HM removal from the soil, there is still room for improvement.

Directions to the Future Research

To create approaches that support better tolerance of HMs in microbes, more emphasis should be placed on understanding the physical, chemical, and biological characteristics of microbes in the prevalence of HMs in soil, water, and gaseous surroundings ( Njoku et al., 2020 ). Furthermore, the application of additives in bioremediation, such as surfactants, might expand the region of the interphase between microorganisms and pollutants, pushing microbes beyond their bioremediation limits. Recently, yeast has been genetically modified to have plant-like properties and to act as hyperaccumulators of several HMs in the aqueous environment ( Sun et al., 2020 ). Other bacteria could be developed in the same way to help in clean-up of HMs. More emphasis should be paid to algae in future study studies, as it is considered an effective microbe for the sorption of HMs from the soil. Because of the better genetic abilities and tolerance to HMs, omics-based techniques are advantageous for the production of improved industrial strains that are tolerant to the prevalent environmental surroundings ( Hemmat-Jou et al., 2018 ). Furthermore, as mentioned in this study, the application of nano- and nano (bio)technologies has enormous ability to promote the use of microbial technologies to deal with HMs pollution. When nanotechnology and microbe-based technology are coupled in environmental restoration procedures, the nanoparticles will promote the elimination of greater pollutant loads, reducing the toxicity-based inhibition of the contaminant on the microbe ( Ma and Zhang, 2008 ). As a result, combining various traditional procedures and current technology could be a potential choice if they could improve relevant material qualities and speed up the restoration process. All life forms and the natural ecosystem are in danger from pollution caused by HMs in soil, water, and agrarian land. Sustainable policies have been developed and revised regularly; nevertheless, awareness of the negative effects, as well as knowledge of how to reduce HMs contaminantion in the soil, should be expanded.

Author Contributions

VP conceptualized and wrote the manuscript. SP wrote the manuscript and made the diagrams. DS wrote the manuscript. PB and MS supervised, helped in writing, reviewing, and editing the manuscript. All authors contributed to the article and approved the submitted version.

We are thankful to the Department of Zoology, Soban Singh Jeena University, Almora (Uttarakhand), India, and DST FIST grant SR/FST/LS-I/2018/131 for providing the facility for this work.

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 : heavy metals, bioremediation, biosorption, biotransformation, bioleaching

Citation: Pande V, Pandey SC, Sati D, Bhatt P and Samant M (2022) Microbial Interventions in Bioremediation of Heavy Metal Contaminants in Agroecosystem. Front. Microbiol. 13:824084. doi: 10.3389/fmicb.2022.824084

Received: 28 November 2021; Accepted: 31 March 2022; Published: 06 May 2022.

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Copyright © 2022 Pande, Pandey, Sati, Bhatt and Samant. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Pankaj Bhatt, [email protected] ; Mukesh Samant, [email protected]

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• Open access
• Published: 27 February 2023

Microbial bioremediation as a tool for the removal of heavy metals

• Mohamed I. Abo-Alkasem   ORCID: orcid.org/0000-0002-0077-6621 1 ,
• Ne’mat H. Hassan 2 &
• Mostafa Mostafa Abo Elsoud 3  

Bulletin of the National Research Centre volume  47 , Article number:  31 ( 2023 ) Cite this article

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The demand for designing a new technology that can emphasize the complete removal of heavy metals increased as a result of the industrial revolution. Bioremediation was found to have a potent impact on the degradation of organic and inorganic environmental pollutants.

Bioremediation is a multidisciplinary technology that possesses safe, efficient, and low-cost characteristics. Also, one of the important features of bioremediation technology is the in-situ treatment which reduces the possibility of transmitting the contaminants to another site. The application of genetic engineering, to engineer a microorganism to acquire the ability to remove different types of heavy metals at a time or to generate a transgenic plant, is considered one of the new promising bioremediation approaches.

Short conclusion

Removal of heavy metal pollution still represents a big challenge for ecologists that’s why this review shed some light on bioremediation technology; its importance, mechanism of action, and prospects.

The world accelerated industrial revolution and the uses of natural resources during metal mining and industry have a great impact on the environment due to heavy metal pollution. Today, one of the most destructive effects facing the world is the contamination with heavy metals, which reaches the air, soil, and water (Asha and Sandeep 2013 ; Raghunandan et al. 2014 , 2018 ). Although trace concentrations of some metals have a vital effect on the health of living organisms, high levels of heavy metals represent toxic effects too (Ahemad 2019 ; Ahuti 2015 ). Also, heavy metals can hardly be degraded in the soil, so their complete detoxification represents a challenge to scientists. Despite the efforts spent to tackle the environmental pollution issue, the world still suffers from the hazardous effects of heavy metals, and so a new technology should be discovered to contain the disaster of heavy metal contamination, one of which is the bioremediation (Raghunandan et al. 2014 , 2018 ).

Several methods have been accomplished to remediate heavy metals pollution, among them Physico-chemical (conventional) methods such as ion exchange, redox, electrochemical techniques, membrane filtration, and precipitation (Nissim et al. 2018 ; Qasem et al. 2021 ). The disadvantages of the conventional methods are the inability of these methods to detoxify heavy metals permanently (Sun et al. 2020 ), in addition to the cost-effectiveness and the hazardous by-products produced by the elimination process. However, the conventional method is considered effective for large areas contaminated with small amounts of heavy metals and for highly polluted local areas (Huët and Puchooa 2017 ). Consequently, building a new technology that emphasizes the complete removal of heavy metals represents a challenge for scientists. Interestingly, microbial remediation of heavy metal has a far-reaching progressive prospect among the decontamination methods. Microorganisms especially soil microbes can tolerate high levels of heavy metals, some microorganisms need certain types of metals as a micronutrient (i.e., Fe 3+ is essentially utilized by all bacteria while Fe 2+ is significant for anaerobic bacteria) to perform their metabolic activities (Ahemad 2019 ). The bioremediation process could be conducted Ex-situ by transferring the contaminated area to be treated or even in situ by delivering the biological source to the polluted land (Shannon and Unterman 1993 ; Naz et al. 2005 ). Most microorganisms follow two common mechanisms in the bioremediation process; metal sequestering or immobilization and enhancement of solubility properties of the metal, other organisms oxidize or reduce the heavy metals to a less toxic form (Donald 2013 ). The bioremediation process also could be accomplished in aerobic and anaerobic environments; however, the aerobic environment was found to be more efficient and faster than anaerobic conditions.

Definition of heavy metals

These can be defined as the elements that have a density higher than 5 g/cm 3 , also the metals or metalloids which have an atomic mass greater than 4000 kg m −3 or 5 times larger than water are considered heavy metals (Paschoalini and Bazzoli 2021 ). A lot of elements fall into this class however, only a few metals (arsenic (As), cadmium (Cd), chromium (Cr), cobalt (Co), copper (Cu), lead (Pb), mercury (Hg), nickel (Ni), tin (Sn), vanadium (V) and zinc (Zn).) commonly existed in the contaminated air, water, and soil. These metals could be found in many forms; insoluble such as carbonate, oxides, silicate, and sulfides, or soluble such as salt forms (Arfala et al. 2018 ), also, heavy metals when persisted in their ionic state (e.g., Cd +2 , Pb +2 , Hg +2 , As +3 ) represent the most toxic form as they combined with bio-molecules and for a complex harder to be dissociated (Duruibe et al. 2007 ). Recently, researchers paid great attention to studying the diffusion phenomenon and mobility through soil layers and in aquifers (Cuevas et al. 2012 ). According to the European Environment Agency reports, industrial process and product use, energy production and distribution, and energy use in industry are the most contributed sectors in the emission of Cd, Hg, and Pb as represented in Fig.  1 . However, road transportation, commercial, institutional, and households have a significant contribution in Pb emission (EEA 2019).

Effect of different life sectors on the emission of Cd, Hg, and Pb in the environment (EEA, 2019 )

Effect of heavy metals on living organisms

Heavy metals with trace concentrations are considered micronutrients that are essential and have nutritional value for some metabolic processes of living cells (Ray and Ray 2009 ), however, elevated levels may have an adverse impact on the health of aquatic and terrestrial living organisms and the environment as they cause dangerous morbidity and mortality (Wang et al. 2006 ; Ray and Ray 2009 ). Heavy metals could be transported to the living cells through the air, water, and food chains and consequently, they alter the physical and chemical properties of the transported material. Heavy metal pollution affects the ecosystem balance by reducing the microbial population of the soil which participates in decomposing the organic material used in crops growing, and so they indirectly affect the food chain of other living organisms, thereby, the world health organization (WHO) and the United States Environmental Protection Agency (USEPA) assigned the acceptable limit for different heavy metals in water as represented in Table 1 . Some metals can destruct living cells directly such as mercury, cadmium, lead, and chromium others have indirect effects such as zinc a corrosive material, and arsenic which pollute catalysts (Hogan 2010 ).

Effect of heavy metals on human

Heavy metals exert their effects by interfering with the function of the organs, however, some of these metals are useful at low concentrations such as arsenic, copper, nickel, iron, etc. (Ray and Ray 2009 ), however, at a high concentration, these metals become cytotoxic as well as carcinogenic for the cells, especially after long term exposure (Jaishankar et al. 2014 ; Valko et al. 2016 ).

Malfunction of human organs is the predominant phenomenon of infected bodies, Zinc for example causes severe gastrointestinal, kidney, brain, respiratory, and heart damage (Hrynkiewicz and Baum 2014 ). Cadmium has the same effect in addition to hypophosphatemia and causes damage to the central nervous system (Hrynkiewicz and Baum 2014 ). Arsenic and mercury damage the liver, the heart, and the central nervous system and cause hypophosphatemia and cancer (Tamele and Vázquez Loureiro 2020 ). Lead which is commonly introduced to the environment in different forms such as mining, lead smelting, ceramic and glass industries, ammunition, storage battery, and tetraethyl-lead manufacturing (Held and Don 2000 ) has a destructive effect on the liver, the heart, and the central nervous system and cause hypophosphatemia, cancer, and anemia (Koning et al. 2001 ; Iranzo et al. 2001 ; Hrynkiewicz and Baum 2014 ). A disastrous disease has already emerged due to heavy metal pollution such as “Itai Itai” in Japan as a result of Cd pollution (Gautam et al . 2015 ), “Arsenecosis” in Bangladesh due to As, and “Minimata” in Japan due to Hg (Volesky 1990 ).

Effect of heavy metals on plants

Physiological dysfunction and malnutrition are the most important disorders that affect plant growth due to excessive concentration of heavy metal pollution, also the disturbance in the ecological balance between plants and microorganisms has a great impact on crops. Malfunctions of the vital physiological processes such as Photosynthesis, and respiration may lead to the degradation of the major organelles following plant death (Glombitza and Reichel 2013 ). As a consequence of the excessive intake of heavy metals by plants, human and animal health will be affected (Babak et al . 2013 ).

Toxicity of heavy metals to the microorganisms

Heavy metals also have a great impact on the growth of microorganisms depending on the type and concentration of the polluted source. Different mechanisms were found to be involved in the toxicity of heavy metals such as dysfunction of enzymatic reactions, production of reactive oxygen species (ROS) which function as soluble electron carries, induction of oxidative damage that may cause changes in DNA and protein formation (Gauthier et al. 2014 ; Hildebrandt et al. 2007 ). Also, heavy metal toxicity affects the transcription and translation of DNA by charging the phosphate group negatively using electrostatic interaction which may cause mutagenesis (Genchi et al. 2020 ), causing acute hurt to the cell membrane and cytoplasmic molecules. Hence, exposure to heavy metals can affect both morphological, biochemical, and physiological properties (Frimmel 2003 ; Fashola et al. 2016 ).

Principles of the bioremediation process

Bioremediation can be defined as the use of biological diversity, directly or indirectly, to convert toxic pollutants into a harmless form (Asha and Sandeep 2013 ), so bioremediation is a holistic approach that includes plant, fungi, bacteria, actinomycetes, and algae all of them could be used as a biological agent to detoxify heavy metals. Two different strategies are utilized to remediate toxic pollutants; in-situ, where the process of decontamination occurred at the contaminated place itself by bringing the biological agent to the site of contamination or promoting the indigenous organisms to deal with contaminants by facilitating the suitable condition for their propagation. The second one is ex-situ , by which the contaminated place is transferred away to another site to be processed (Kumar et al. 2011a , b ; Kumar et al. 2016 ; Raghunandan et al. 2014 , 2018 ). There are many mechanisms by which the organism can manipulate the detoxification process, however, the utilization of the toxic metal by the microorganism as a source of nutrition is the main concept (Sun et al. 2020 ). So, microbial bioremediation is considered a multidisciplinary field that required more research and investigations.

Types of bioremediations

Bioremediation is classified, according to the site at which the bioremediation process occurred, into two different strategies:

• In-situ bioremediation

This strategy corresponded with treating the polluted surfaces where they are located, this strategy depends on detoxifying the dissolved and sorbed pollutants directly by the microorganism, it can be applied in groundwater, unsaturated and saturated soils, also it is considered an efficient method to remediate organic chemicals in contrary to ex-situ strategy (Brar et al. 2006 ), also in-situ bioremediation expanded to treat inorganic and toxic metals. Moreover, the application of microorganisms that have a chemotactic ability to facilitate moving into the contaminated areas and hence the degradation of harmful compounds will be safer (Kulshreshtha et al. 2014 ). Furthermore, stimulating the reduction of heavy metals at the place minimizes the chance of contaminant transportation downgradient. A challenging issue facing in-situ bioremediation is the selection of one organism or a consortium of organisms that has the potential ability to detoxify the targeted metals. In lab-scale, it was found that Fe 3+ and sulfate-reducing microorganisms have the enzymatic ability to biodegrade some heavy metals such as U(VI), Tc (VIII), Cr (VI), and Co (III) (Gorby et al. 1998 ; Tebo and Obraztsova 1998 ; Lloyd et al. 2000 ). Also, species of Geobacteraceae were found to be a dominant group during the stimulation process for reducing Fe 3+ , also, the members of this group were detected in the stimulation process to reduce U(VI) of contaminated Aquifer. So, the Geobacteraceae group was considered to play an important role in stabilizing contaminants and reducing metals within subsurface environments (He et al. 2019 ). The following are some techniques used for “in-situ” bioremediation:

Biosparging

Biosparging system is Constructed by injecting the air through a pipe below the water table which enhances the growth of indigenous microbes due to elevated oxygen concentration (Jain et al. 2012 ). Also, it differs from bioventing in mixing the soil and the groundwater by injecting the air in the saturated area, which allows the movement of volatile organic compounds upward to the unsaturated area this process is affected by the biodegradability of the contaminants and soil characteristics. This system possesses low construction cost and flexibility in adapting the design (Atlas and Philp 2005 ).

Bioventing is a system that stimulates the existing soil microorganisms to degrade the source of pollution via injecting a limited amount of oxygen that sustains microbial activity (Jain et al. 2012 ). Injection of air is conducted in the unsaturated area in addition to supplementing it with nutrients and moisture (Philp and Atlas 2005). Bioveting could be more efficient in anaerobic biodegradation, also mixing nitrogen with oxygen will increase the potency of chlorinating remediation (Mihopoulos et al. 2000 , 2002 ; Shah et al. 2001 ).

Bioaugmentation

Bioaugmentation is the application of outsourcing microbial strains that naturally occurred or are genetically engineered to decontaminate polluted soil or water. Treatment usually utilizes a consortium of microorganisms that produce all the required enzymes and degradative pathways. Bioaugmentation is used to treat municipal wastewater, soil, and groundwater polluted with chlorinated ethenes which are degraded to nontoxic ethylene and chloride (Jain et al. 2012 ).

Intrinsic bioremediation

Intrinsic bioremediation is defined as the stimulation of naturally occurring organisms by providing nutritional materials and oxygen to remediate heavy metals without attribution of any engineering steps (Riseh et al. 2022 ).

Engineered bioremediation

Engineered bioremediation is the adaptation of physicochemical conditions to enhance the propagation of introduced microorganisms to accelerate the bioremediation process.

Advantage of in-situ bioremediation

Cost-effectiveness of in-situ bioremediation

It can be used to treat large contaminated areas which could reach inaccessible regions.

Treating a wide variety of wastes, it may be used the decontaminate organic and inorganic wastes.

In-situ bioremediation is faster than the pump-and-treat method.

Challenges facing in-situ bioremediations

Limitations in depending on indigenous microorganisms as their metabolic activity could be inhibited by high levels of heavy metals.

Some pollutants may be bio-transformed due to microbial metabolic activity to an intermediate which could be more toxic and mobile than the original form.

In-situ bioremediation could be inappropriate in treating some contaminants such as recalcitrant.

In-situ bioremediation is most suitable for low-level scenarios of pollution (Kulshreshtha et al. 2014 ).

• Ex-situ bioremediation

The core concept of this strategy is to treat the contaminated site by the excavation of soil to enhance microbial degradation. Five techniques were used in this strategy.

Slurry-phase

This technique relies on excavating the contaminated soil and mixing it with water and transporting the mixture to a bioreactor, followed by stone and rubble removal. The amount of water depends on the pollutant's type and concentration, the soil's nature, and the biodegradation rate. This process is followed by the separation of the soil by filtration or centrifugation, the soil is dried and retransferred to its original location, and the fluids are submitted to a further treatment step (EPA 2003 ).

Solid-phase

This technique involves three steps: excavation of the soil, followed by putting the soil into piles, the soil may contain municipal, agricultural, and organic wastes, followed by stimulation of the biodegradation process by supplying oxygen through a network of pipes to enhance microbial respiration and subsequently microbial activity. Solid-phase bioremediation requires a large space and a long time to be completed (Hyman and Dupont 2001 ).

Landfarming

This technique relies on the stimulation of indigenous organisms spread over the surface by supplementing the excavated soil with suitable nutrients and minerals, the excavated soil should be periodically tilled to stimulate the biodegradation process.

Soil biopiles

This technique is almost similar to landfarming bioremediation except in using above-ground piles and perforated pipes to inject air through the soil (Verma 2022 ). Application of this technique is interestingly valuable because of its low cost and full control of nutritional feed, aeration, and temperature (Whelan et al. 2015 ), also it’s the technique of choice in treating contaminated sites of extreme environments and in treating low molecular weight compounds by limiting volatilization (Gomez and Sartaj 2014 ).

Composting bioremediation

Composting bioremediation is quite similar to landfarming bioremediation in excavating the contaminated soil to the surface and stimulating the indigenous microorganisms through feeding of nutrients and injecting air but differs in supplementing the soil with a bulk of additives such as corncobs, straw, and hay, this additive helps in oxygen distribution through the soil, maintaining the moisture content constant and turning frequency, however, application of composting process for biodegradation of volatile pollutants is not favorable because of the periodic turning during the process (Hobson et al. 2005 ).

Advantage of ex-situ bioremediation

Adequate control of the biodegradation process.

Suitability to detoxify a wide variety of contaminants.

Reduction of time required to complete the treatment process.

Challenges facing ex-situ bioremediation

Limitation of ex-situ bioremediation to biodegrade chlorinated hydrocarbons.

Some types of soils required further processing such as non-permeable soils.

Bioremediation mechanism of action

Due to the ubiquitous nature of microorganisms, they play a crucial role in the bioremediation of heavy metals, they can interact with heavy metals using different mechanisms to survive the toxicity of the metals. The two main concepts by which the organism can deal with contaminants are using the contaminant as a source of nutrition and protecting the organism itself (defense mechanism) from the toxic effect ( Alvarez et al. 2017 ). As illustrated in Fig.  2 , the microorganism reacts with the environmental contaminants using direct or indirect mechanisms some of which are biosorption and biotransformation (Tang et al. 2021 ).

Diagram showing different mechanisms of bioremediation action

• Biosorption

It’s a mechanism by which the organism binds with the metal to form a complex that possesses a nontoxic feature. Certain criteria should be considered and investigated to achieve a potential biosorption mechanism; nature of the biosorbent, sorption capacity, kinetics of sorption, regeneration ability of the sorbent, percentage of metal recovery, cost-effectiveness of biosorption process, and separation flexibility of the biosorbent-metal complex (Bae et al. 2001 , 2002 , 2003 ). Two main categories are involved in the bioremediation process using the biosorption mechanism.

Metabolism-independent biosorption

This type of biosorption depends on the physical and chemical properties of the cell whether it was a live cell or a dead cell, this category involves the following:

Adsorption, also called extracellular sequestration, relies on the affinity between cellular components of the periplasm and the metal ion. Extracellular polymeric substance (EPS) associated with bacterial cell wall plays a significant role in metal adsorption. EPS is composed of polysaccharides, mucopolysaccharides, and proteins. It also contains a lot of functional groups (hydroxyl, carboxyl, amine, and phosphoric groups) that facilitate heavy metal sequestering (Guine et al . 2006 ).

Affinity and ion exchange by which the biosorbent (cellular component) binds with the metal ion, Cunninghamella were found to have a promising binding ability to heavy metals released textile wastewater (Tigini et al. 2010 ), also Saccharomyces cerevisiae can degrade Cd(II) and Zn(II) using the ion-exchange method.

Efflux system as a type of extracellular sequestration is one of the most important methods by which the organism can defend against the toxic effect of heavy metals by forming an outer protective material and ejecting the metal ion out of the cytoplasm to the periplasmic region (Dixit et al. 2015 ). Ma et al. ( 2016 ) reported that transformation and efflux are the basic methods usually used in bacterial resistance to heavy metals.

Metabolism-dependent biosorption

This mechanism is associated with the metabolic activity of a viable microorganism contrary to metabolism-independent biosorption.

Intracellular sequestering (Bioaccumulation), is a process by which the complex form of cell-metal occurred inside the cytoplasm (Ramasamy and Banu 2007 ), as reported by (Abo-Alkasem et al. 2022a ) and illustrated in Fig.  3 , examination of Salipaludibacillus agaradhaerens  strain NRC-R cells using the Transmission Electron Microscope (TEM) showed the accumulation of chromium inside the cell which also confirmed by EDX analysis, accumulation of metals conducted by attaching with the cell surface follows slow penetration to periplasm to the cell cytoplasm by a process that looks like nutrient uptake (Mishra and Malik 2013 ), it was reported that cysteine-rich protein plays an important role in sequestering Zn, Cd, and Cu in cadmium-tolerant Pseudomonas putida, also, glutathione helps in sequestering Cd by Rhizobium leguminosarum. Fungi also play a vital role in inorganic metal elimination using their rigid cell wall which works as a ligand in the decontamination process.

TEM image of the cells grown in the presence of Cr (VI) (Abo-Alkasem et al. 2022a )

Siderophore-mediated biosorption, also called a chelating agent, in aerobic soils some microorganisms produce siderophores that mediate the ability of the microorganisms to utilize low water-soluble metals using an energy-dependent process (John et al. 2001 ). Microbacterium flavescens was found to use siderophore to uptake their nutritional requirements of iron, also the organism uses the siderophore desferrioxamine-(DF) to bind with uranium, plutonium, and iron.

• Biotransformation

Biotransformation relies on the cellular metabolic activity of the microorganism through the redox mechanism, reduction of metals by changing the oxidation number of the metal is common in nature, such as the reduction of chromium (Abo-Alkasem et al. 2022a , b ), selenium (Lloyd et al. 2001 ), uranium (Chang et al. 2001 ) and mercury (Brim et al. 2000 ).

Oxidation and reduction mechanisms

The mechanism by which the microorganism works as an oxidizing agent by releasing electrons that react with the anions in the contaminated soil is the same mechanism utilized to decontaminate organic compounds under anaerobic conditions (Lovley and Phillips 1988 ). However, it was found that the presence of iron (III) stimulates the degradation process (Spormann and Widdel 2000 ). The reduction could be occurred directly using a bioreactor, (pump and treat) or after the excavation of soils, inoculated with the appropriate microbial consortium, or indirectly using sulfate-reducing bacteria which plays an important role in the ecological balance directly by sulfate reduction or indirectly by the formation of biofilms (Abo Elsoud and Abo-Alkasem 2022 ). The indirect mechanism is more favorable due to its cost-effectiveness and eco-friendly method (Asha and Sandeep 2013 ). Decontamination of uranium by Desulfosphorosinus spp. And Closteridium spp is an applicable example of utilizing sulfate-reducing bacteria (Prasad and Freitas 2003 ).

Methylation of metals (volatilization)

Volatilization of metal by microbial methylation plays a significant role in metal remediation, for instance, some Pseudomonas spp., Escherichia spp., Clostridium spp . , and Bacillus spp . can convert Hg (II), Se, As, and Pb to a gaseous methylated form (Ramasamy and Banu 2007 ).

Bioleaching

Bioleaching is the secretion of low molecular weight compounds that aid the transformation of a toxic form of metals to a nontoxic form by dissolution or precipitation mechanisms, (Chanmugathas and Bollag 1988 ) reported that leaching of Cd is promoted by the secretion of organic acids by some microorganisms, also the production of inorganic phosphate by Citrobacter organism leads to precipitation of metal phosphate coat.

Plant-microbial remediation

Rhizoremediation is the association of microorganisms with plants to improve the potential of the bioremediation process and it now plays a crucial role in environmental bioremediation due to cost-effectiveness and outstanding efficiency (Nie et al. 2011 ; Marihal and Jagadeesh 2013 ; Prabha et al. 2017 ).

The capability of microorganisms to develop a symbiotic relationship enhances the biodegradability of different types of contaminants (Kumar et al. 2017 ). The predominant type of organisms associated with the plant-microorganism relationships is mycorrhizal fungi which can bio-sorb heavy metals (Bojorquez and Voltolina 2016 ). The potentiality of rhizoremediation was reported by Joner and Leyva ( 1997 ) who found that mycorrhizal plants when subjected to soil contaminated with Cd 2+ 1, 10, and 100 mg/kg, Cd uptake of mycorrhizal was higher than non-mycorrhizal plants by 90%, 127%, and 131% respectively. The mechanisms utilized in rhizoremediation are mainly through the activation of metal phosphates, acidification, production of organic acids, chelating agents, and ion carriers.

Microorganisms responsible for bioremediation

In nature, the presence of microorganisms guarantees the retrieval of ecological balance and the removal of contaminants that hinder biological life. The use of microorganisms for the removal of contaminants from the environment is described as "Bioremediation". The concept of environmental remediation using microorganisms was first registered as a patent in 1981 for the degradation of petroleum oil by Pseudomonas putida (Prescott et al. 2002 ; Glazer and Nikaido 2007 ). Bioremediation aims to stimulate microbial metabolic activity, with nutrients or other chemical agents, to be able to remove, destroy, or neutralize the effect of these contaminants. The microorganisms used for bioremediation should not only be able to tolerate a wide concentration range of the contaminant(s) but also be physiologically active. Once favorable conditions are obtained, the metabolic activity and growth rate of these microorganisms reach alarming levels as well as the bioremediation process. Many theories have been illustrated for the mechanism of microbial tolerance to heavy metals. These theories include the accumulation and formation of non-toxic complexes with the metal ions inside the cells, the efflux of toxic metals outside the cell, biotransformation of the toxic metal into a less toxic form, or methylation and/or de-methylation.

In nature, the type of micro-flora (microbial consortium) is a significant factor affecting the tolerance and rate of heavy metal bioremediation depending on the gene and metabolic diversity (Juwarkar et al. 2010 ). Two types of microorganisms are used for heavy metal bioremediation based on their sources: indigenous (microorganisms present in the site of contamination and have bioremediation capability) and extraneous (microorganisms introduced into the site of contamination and have bioremediation capability), Table 2 summarizes some of the organisms used in the bioremediation process and their target pollutants. The utilization of indigenous microorganisms excludes the need for continuous monitoring according to Asha and Sandeep ( 2013 ). After the bioremediation process, the soil and/or water retrieve their ability to be reused in various activities.

It was reported that many microorganisms including bacteria, Actinomycetes, fungi, yeast, and algae can remediate heavy metals from soil and water:

Endophytic bacteria and Plant Growth Promoting Rhizobacteria (PGPR) are the most common bacterial strains associated with heavy metal bioremediation.

The endophytic bacteria colonize the sub-epidermal layer of the plant tissues (Schulz and Boyle 2006 ). The presence of endophytic bacteria helps the protection of the plant cells from heavy metals stress conditions (Ryan et al. 2008 ). They diminish or remove the phytotoxicity of the heavy metals by altering their phyto-availability (Weyens et al. 2009 ; Ma et al. 2011 ) such as some species of Pseudomonas, Bacillus, and Rahnella that showed high resistance to Pb, Mn, and Cd (Luo et al. 2012 ; Yuan et al. 2014 ; Babu et al. 2015 ).

On the other hand, PGPR comprises a group of free-living, symbiotic, or endophytic bacteria (Glick 2012 ). For example, Bacillus, Enterobacter, Erwinia, Flavobacterium, Klebsiella, Gluconacetobacter, and Pseudomonas (Nadeem et al. 2010 ) can mitigate the toxicity of heavy metals, improve plant growth in heavy metal-contaminated soils (Seth 2012 ) and produce phytohormones and siderophores and help phosphate solubilization (Ullah et al. 2015 ).

Actinobacteria

In addition to their well-known ability to utilize complex organic matter as a carbon and energy source (Kieser et al. 2000 ), Actinobacteria, such as Amycolatopsis , Corynebacterium, Rhodococcus, and Streptomyces , can tolerate and remediate heavy metals, such as Hg(II), Co(II), Cd(II), Cr(VI), Zn(II) and Ni(II) (Oyetibo et al. 2010 ; Alvarez et al. 2017 ).

Some fungal strains have been reported to possess metal chelating and sequestrating systems that increase their heavy metal tolerance and biotransformation into a less toxic form such as Allescheriella, Pleurotus, Phlebia, and Stachybotrys (D’Annibale et al. 2007 ). The hyphal and high biomass growth adds an advantage to this type of microorganism as it allows simple harvest along with the attached heavy metals (Aly et al. 2011 ). Aspergillus, Penicillium, Cephalosporium, and Rhizopus are the most studied fungal genera for their potential activity in the removal of heavy metals, such as Pb 2+ and Zn 2+ , from aqueous solutions and soils (Volesky and Holan 1995 ; Huang and Huang 1996 ; Tunali et al. 2006 ; Akar et al. 2007 ).

Factors affecting the bioremediation process

To confine the biodegradation potential on selecting the most appropriate method, mechanism, and technique without paying attention to the factors that may affect the utilized application, limit the efficiency of the bioremediation process. A lot of factors could exhibit significant effects on the bioremediation process, for instance, metal ion concentration, valance state and chemical forms of the metal, the bioavailability of the metal, redox potential, availability of low molecular weight organic acids, and environmental factors such as temperature and pH (Bandowe et al. 2014 ).

Substrate concentration

To establish the process of bioremediation, bio-sorbent accumulation features should be quantified, two models could be used; the Langmuir model mainly defines adsorption by assuming an adsorbate behaves of the single-layer (Acar and Malkoc 2004 ), and the Freundlich model which mainly estimates the adsorption equilibrium (Febrianto et al. 2009 ). However, the main concept is that the adsorption efficiency increases with the increment of heavy metal concentration until a certain value.

Type of the substrate

The efficiency of the adsorption mechanism is affected by the type of soil, the type of heavy metal, and the type of soil additives. since the adsorption between the soil and heavy metals may lower the mobility of heavy metals and hence reduce microbial adsorption (Hu et al. 2010 ). Also, soil additives have a significant effect on heavy metals removal, Tyagi et al. ( 2014 ) found that increasing FeSO 4 .7H 2 O higher than 20 gm/l has an adverse effect on the leaching rate of Cu and Zn.

The potential of hydrogen (pH) plays a vital role in both microbial activity and metal characteristics. Growing of microorganisms in unfavorable pH may affect the enzyme activity thereby lowering the rate of microbial metabolism, also, the charge of the microorganism surface will be changed that affects the binding capacity between the adsorbent and heavy metals (Bandowe et al. 2014 ; Galiulin and Galiulina 2008 ). Furthermore, changes in pH value may alter metal mobility and hydration as the metals tend to be free ionic at acidic pH (Bandowe et al. 2014 ; Dermont et al. 2008 ). According to (Rodríguez-Tirado et al. 2012 ; Wierzba 2015 ), the adsorption capacity of Pb 2+ and Zn 2+ increased by raising the pH value to 5.5, however, an observed decrease in the removal of metals was recorded upon increasing pH value over (5.5).

Temperature

Temperature is an important parameter in adjusting the optimum conditions for microbial growth, metabolism, and enzyme activity (Fang et al. 2011 ), increasing temperature affects the diffusion of metals across different layers and also, increases the bioavailability of metals. However, the optimum biodegradation temperature differs according to the type of metal, for instance, the biodegradation of Cd 2+ by Bacillus jeotgali was the highest at 35 °C, however, it was 30 °C for Zn 2+ biodegradation (Chanmugathas and Bollag 1988 ).

Role of biotechnology in the bioremediation process

Biotechnology is the discipline of using the engineering of scientific principles to improve the efficiency of organisms to serve humans and remediate the environmental toxic substance (McHughen 2016 ), by using genetic engineering, one of the biotechnology approaches, a single organism can be engineered to produce all the needed enzymes or to utilize all the degradative pathways for bioremediation process (Dangi et al. 2019 ). The purpose of utilizing genetic tools is to enhance efficiency and reduce the cost and time of the bioremediation process.

Degradation of Polychlorinated biphenyls (PCBs) is controlled by to group of genes that were found in the genetic material of two different organisms, thereby, using genetic engineering for achieving recombination between Pseudomonas pseudoalcaligenes KF707 and Burkholderia cepacia LB400 bph genes may enhance the degradation rate of PCBs and stimulate the remediation of toluene and benzene (Seeger et al. 2010 ), also the application of DNA probes helps in accelerating the process of the isolation and identification of a particular strain from a mixed population (Dua et al. 2002 ). Another example of using biotechnology is the fusion between metallothionein (MT) isolated from rats, IgA protease protein isolated from Neisseria gonorrhoeae, and the fusion vehicle lpp-ompA to provide the bacterial cell wall with metal ion-binding polypeptides (Bae et al. 2000 and Valls et al. 2000 ).

Another discipline of biotechnology involves the use of transgenic plants in the bioremediation process, this could be conducted by transferring a desirable gene from different sources (other plants, microorganisms, or even animals) to improve the ability of the plant to remove the toxic pollutant (Truu et al. 2015 ) this process of transmission increases the phytoremediation ability of the plant (Dixit et al. 2015 ).

Immobilized microorganism technology

Immobilization is one utilized technique in bioremediation, it possesses stability of the biological cell, also the immobilized cell did not compete with indigenous organisms, therefore it is considered eco-friendly and has high degradation efficiency (lone et al. 2008 ).

Advantage of bioremediation

A natural bioprocess is characterized by a safe effect on the environment which makes it globally accepted as a technique for treating wastes.

The consumed energy is lower than the technologies.

Cost-effectiveness is one of the most bioremediation features.

Several types of pollutants could be eliminated at the same time.

Minimize the risk of transferring the contamination from one site to another.

Disadvantages of bioremediation

Several factors could affect the efficiency of the bioremediation process.

Elimination of toxic metals to be achieved could take a lot of time.

Limited to those contaminates that can be biodegradable.

Biodegradation capacity and efficiency cannot be predicted because of dealing with a live organism (Zeyaullah et al. 2009 ).

Conclusions

Great efforts were spent during the last few decades to address the problem of heavy metal pollution by developing new strategies to fix this issue, however, the application of bioremediation techniques still represents the most favorable strategy due to the cost-effectiveness and safety impacts of bioremediation techniques on the environment and also due to the variability of bioremediation mechanisms which makes these techniques applicable and affordable, this article enumerates different types of bioremediation and the advantage and disadvantage of these types also the suitability of these types to different environments and conditions moreover, the article summarizes some of the mechanisms of action of different bioremediation techniques in addition to the microorganisms that play an important role and the factors that may affect the bioremediation process and how the newly developed technologies can improve the bioremediation techniques to be more efficient.

Availability of data and materials

Not applicable.

Abbreviations

Deoxyribonucleic acid

Desferrioxamine

Extracellular polymeric substance

Plant Growth Promoting Rhizobacteria

Polychlorinated biphenyls

Reactive oxygen species

The United States Environmental Protection Agency

World Health Organization

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Abo-Alkasem, M.I., Hassan, N.H. & Abo Elsoud, M.M. Microbial bioremediation as a tool for the removal of heavy metals. Bull Natl Res Cent 47 , 31 (2023). https://doi.org/10.1186/s42269-023-01006-z

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Recent trends on bioremediation of heavy metals; an insight with reference to the potential of marine microbes

• Published: 12 May 2024

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• S. Sonker 1 , 2 ,
• A. B. Fulke 1 , 2 &
• A. Monga 3  

Heavy metals are essential for the survival of all living organisms in trace amounts. Industrializations and urbanisation are the two major rationale behind the massive rise in the contamination of land and water bodies including marine and freshwater. The major sources of heavy metal are coal burning, smelting operations, tanneries, waste incineration, pesticides, fungicides, metallurgy, etc. Due to the toxicity of heavy metals when living beings encounter contaminated water of sediment laden with heavy metal endure health hazards. Heavy metals and metalloids such as chromium, lead, mercury, cadmium, nickel, and cobalt are poisonous and carcinogenic even in minute amounts, posing a major threat to human life. The most sustainable approach towards remediating these heavy metals is bioremediation. It involves bacterial bioremediation, fungal, biofilms and phytoremediation, which is not only sustainable but also efficient and cost effective. This review delivers a comprehensive overview of the recent trends in bioremediation of heavy metals, their sources, toxicity, and alternative approach of using marine microbes and their pottential for remediation of heavy metals.

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Acknowledgements

Authors are grateful to Director, CSIR-National Institute of Oceanography (CSIR-NIO), Goa, India and Scientist-in-Charge, CSIR-NIO, Regional Centre, Mumbai and Academy of Scientific and Innovative Research (AcSIR) for their encouragement and support.

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Sonker, S., Fulke, A.B. & Monga, A. Recent trends on bioremediation of heavy metals; an insight with reference to the potential of marine microbes. Int. J. Environ. Sci. Technol. (2024). https://doi.org/10.1007/s13762-024-05673-x

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Received : 08 September 2023

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Published : 12 May 2024

DOI : https://doi.org/10.1007/s13762-024-05673-x

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