Genetic basis and importance of metal resistant genes in bacteria for bioremediation of contaminated environments with toxic metal pollutants

Metal pollution is one of the most persistent and complex environmental issues, causing threat to the ecosystem and human health. On exposure to several toxic metals such as arsenic, cadmium, chromium, copper, lead, and mercury, several bacteria has evolved with many metal-resistant genes as a means of their adaptation. These genes can be further exploited for bioremediation of the metal-contaminated environments. Many operon-clustered metal-resistant genes such as cadB, chrA, copAB, pbrA, merA, and NiCoT have been reported in bacterial systems for cadmium, chromium, copper, lead, mercury, and nickel resistance and detoxification, respectively. The field of environmental bioremediation has been ameliorated by exploiting diverse bacterial detoxification genes. Genetic engineering integrated with bioremediation assists in manipulation of bacterial genome which can enhance toxic metal detoxification that is not usually performed by normal bacteria. These techniques include genetic engineering with single genes or operons, pathway construction, and alternations of the sequences of existing genes. However, numerous facets of bacterial novel metal-resistant genes are yet to be explored for application in microbial bioremediation practices. This review describes the role of bacteria and their adaptive mechanisms for toxic metal detoxification and restoration of contaminated sites.

[1]  M. C. Vargas-García,et al.  Compost as a source of microbial isolates for the bioremediation of heavy metals: in vitro selection. , 2012, The Science of the total environment.

[2]  M. Saier,et al.  CHR, a Novel Family of Prokaryotic Proton Motive Force-Driven Transporters Probably Containing Chromate/Sulfate Antiporters , 1998, Journal of bacteriology.

[3]  Ning Wang,et al.  ArsH from Synechocystis sp. PCC 6803 reduces chromate and ferric iron. , 2014, FEMS microbiology letters.

[4]  M. Amoroso,et al.  Copper removal ability by Streptomyces strains with dissimilar growth patterns and endowed with cupric reductase activity. , 2008, FEMS microbiology letters.

[5]  S. Silver,et al.  A second gene in the Staphylococcus aureus cadA cadmium resistance determinant of plasmid pI258 , 1991, Journal of bacteriology.

[6]  Thomas V. O'Halloran,et al.  Identification of a Copper-Responsive Two-Component System on the Chromosome of Escherichia coli K-12 , 2000, Journal of bacteriology.

[7]  Wilfred Chen,et al.  Engineering Plant-Microbe Symbiosis for Rhizoremediation of Heavy Metals , 2006, Applied and Environmental Microbiology.

[8]  G. Archana,et al.  Cytosolic expression of synthetic phytochelatin and bacterial metallothionein genes in Deinococcus radiodurans R1 for enhanced tolerance and bioaccumulation of cadmium , 2014, BioMetals.

[9]  T. Greenland,et al.  Nucleic acid sequence and affiliation of pLUG10, a novel cadmium resistance plasmid from Staphylococcus lugdunensis. , 1996, Plasmid.

[10]  R. Naidu,et al.  Concomitant rock phosphate dissolution and lead immobilization by phosphate solubilizing bacteria (Enterobacter sp.). , 2011, Journal of environmental management.

[11]  D. Nies,et al.  Efflux-mediated heavy metal resistance in prokaryotes. , 2003, FEMS microbiology reviews.

[12]  P. Lejeune,et al.  “NiCo Buster”: engineering E. coli for fast and efficient capture of cobalt and nickel , 2014, Journal of biological engineering.

[13]  A. Kornberg.  Inorganic polyphosphate: toward making a forgotten polymer unforgettable , 1995, Journal of bacteriology.

[14]  M. Solioz,et al.  Copper homeostasis in Enterococcus hirae. , 2003, FEMS microbiology reviews.

[15]  Lingxin Chen,et al.  Characterization of a marine-isolated mercury-resistant Pseudomonas putida strain SP1 and its potential application in marine mercury reduction , 2012, Applied Microbiology and Biotechnology.

[16]  Dorothea K. Thompson,et al.  High-level chromate resistance in Arthrobacter sp. strain FB24 requires previously uncharacterized accessory genes , 2009, BMC Microbiology.

[17]  Prof. M.R Shakibaie,et al.  CADMIUM BIOREMEDIATION BY METAL-RESISTANT MUTATED BACTERIA ISOLATED FROM ACTIVE SLUDGE OF INDUSTRIAL EFFLUENT , 2010 .

[18]  M. Dinauer,et al.  Cupric Yersiniabactin Is a Virulence-Associated Superoxide Dismutase Mimic , 2013, ACS chemical biology.

[19]  J. DiRuggiero,et al.  Cloning and Sequence Analysis of the Mercury Resistance Operon of Streptomyces sp. Strain CHR28 Reveals a Novel Putative Second Regulatory Gene , 2000, Journal of bacteriology.

[20]  A. Imberty,et al.  Spectroscopic characterization of the metal-binding sites in the periplasmic metal-sensor domain of CnrX from Cupriavidus metallidurans CH34. , 2011, Biochemistry.

[21]  T. Tetaz,et al.  Plasmid-controlled resistance to copper in Escherichia coli , 1983, Journal of bacteriology.

[22]  A. Chung,et al.  The Chromate-Inducible chrBACF Operon from the Transposable Element TnOtChr Confers Resistance to Chromium(VI) and Superoxide , 2008, Journal of bacteriology.

[23]  James K. Fredrickson,et al.  Engineering Deinococcus geothermalis for Bioremediation of High-Temperature Radioactive Waste Environments , 2003, Applied and Environmental Microbiology.

[24]  M. Mergeay,et al.  Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans Are Specialized in the Maximal Viable Response to Heavy Metals , 2007, Journal of bacteriology.

[25]  Surajit Das,et al.  Extracellular polymeric substances of a marine bacterium mediated synthesis of CdS nanoparticles for removal of cadmium from aqueous solution. , 2016, Journal of colloid and interface science.

[26]  Anna Obraztsova,et al.  Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors , 1998 .

[27]  Christian von Mering,et al.  STRING 7—recent developments in the integration and prediction of protein interactions , 2006, Nucleic Acids Res..

[28]  A. Rehman,et al.  Cadmium resistance mechanism in Escherichia coli P4 and its potential use to bioremediate environmental cadmium , 2015, Applied Microbiology and Biotechnology.

[29]  E. Chartone-Souza,et al.  Operon mer: bacterial resistance to mercury and potential for bioremediation of contaminated environments. , 2003, Genetics and molecular research : GMR.

[30]  C. Cervantes,et al.  Reduction and Efflux of Chromate by Bacteria , 2007 .

[31]  A. Pühler,et al.  The genetic organization and evolution of the broad host range mercury resistance plasmid pSB102 isolated from a microbial population residing in the rhizosphere of alfalfa. , 2001, Nucleic acids research.

[32]  Michael B. Yaffe,et al.  Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs , 2003, Nucleic Acids Res..

[33]  Zofia Piotrowska-Seget,et al.  Lead resistance in micro-organisms. , 2014, Microbiology.

[34]  Surajit Das,et al.  Characterization and cadmium-resistant gene expression of biofilm-forming marine bacterium Pseudomonas aeruginosa JP-11 , 2014, Environmental Science and Pollution Research.

[35]  X. Deng,et al.  Subcellular targeting of bacterial CusF enhances Cu accumulation and alters root to shoot Cu translocation in arabidopsis. , 2014, Plant & cell physiology.

[36]  D. Nies,et al.  Cupriavidus metallidurans: evolution of a metal-resistant bacterium , 2009, Antonie van Leeuwenhoek.

[37]  H. Ceri,et al.  Mixed-Species Biofilms Cultured from an Oil Sand Tailings Pond can Biomineralize Metals , 2014, Microbial Ecology.

[38]  H. R. Dash,et al.  Characterization and potential application in mercury bioremediation of highly mercury-resistant marine bacterium Bacillus thuringiensis PW-05 , 2014, Environmental Science and Pollution Research.

[39]  Y. Yun,et al.  Bacterial biosorbents and biosorption. , 2008, Biotechnology advances.

[40]  C. Ouzounis,et al.  Expansion of the BioCyc collection of pathway/genome databases to 160 genomes , 2005, Nucleic acids research.

[41]  Z. Piotrowska-Seget,et al.  Molecular basis of active copper resistance mechanisms in Gram-negative bacteria , 2013, Cell Biology and Toxicology.

[42]  B. Whitton,et al.  Prokaryotic metallothionein gene characterization and expression: chromosome crawling by ligation-mediated PCR , 1990, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[43]  M. Naik,et al.  Pseudomonas aeruginosa strain WI-1 from Mandovi estuary possesses metallothionein to alleviate lead toxicity and promotes plant growth. , 2012, Ecotoxicology and environmental safety.

[44]  P. Sadler,et al.  Multiple bacteria encode metallothioneins and SmtA‐like zinc fingers , 2002, Molecular microbiology.

[45]  T. Barkay,et al.  Microbial transformations of mercury: potentials, challenges, and achievements in controlling mercury toxicity in the environment. , 2005, Advances in applied microbiology.

[46]  R. Naidu,et al.  Molecular characterization of chromium (VI) reducing potential in Gram positive bacteria isolated from contaminated sites , 2010 .

[47]  I. Pepper,et al.  Dual-Bioaugmentation Strategy To Enhance Remediation of Cocontaminated Soil , 2001, Applied and Environmental Microbiology.

[48]  J. M. Dow,et al.  The versatility and adaptation of bacteria from the genus Stenotrophomonas , 2009, Nature Reviews Microbiology.

[49]  M. Mandrand-Berthelot,et al.  Identification of rcnA (yohM), a Nickel and Cobalt Resistance Gene in Escherichia coli , 2005, Journal of bacteriology.

[50]  D. Lovley,et al.  Bioremediation of metal contamination. , 1997, Current opinion in biotechnology.

[51]  S. Cameotra,et al.  In Silico Approach for the Bioremediation of Toxic Pollutants , 2013 .

[52]  Lars Järnström,et al.  Comparison of lignin derivatives as substrates for laccase-catalyzed scavenging of oxygen in coatings and films , 2014, Journal of biological engineering.

[53]  A. Al-Gheethi,et al.  Biosorption of nickel by Pseudomonas cepacia 120S and Bacillus subtilis 117S. , 2010, Water science and technology : a journal of the International Association on Water Pollution Research.

[54]  S. Silver,et al.  Generation of Mercury-Hyperaccumulating Plants through Transgenic Expression of the Bacterial Mercury Membrane Transport Protein MerC , 2006, Transgenic Research.

[55]  N. Brown,et al.  Sequence and Analysis of a Plasmid-Encoded Mercury Resistance Operon from Mycobacterium marinum Identifies MerH, a New Mercuric Ion Transporter , 2008, Journal of bacteriology.

[56]  A. Rosado,et al.  Diversity of Mercury Resistant Escherichia coli Strains Isolated from Aquatic Systems in Rio de Janeiro, Brazil , 2013 .

[57]  Peer Bork,et al.  SMART 5: domains in the context of genomes and networks , 2005, Nucleic Acids Res..

[58]  R. García-Ruiz,et al.  Utilizing Microbial Community Structure and Function to Evaluate the Health of Heavy Metal Polluted Soils , 2010 .

[59]  M. Solioz,et al.  Copper homeostasis in Enterococcus hirae. , 1999, Advances in experimental medicine and biology.

[60]  J. Imlay,et al.  The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity , 2009, Proceedings of the National Academy of Sciences.

[61]  M. Naik,et al.  Biological characterization of lead-resistant bacteria to explore role of bacterial metallothionein in lead resistance , 2012 .

[62]  G. Nucifora,et al.  Cadmium resistance from Staphylococcus aureus plasmid pI258 cadA gene results from a cadmium-efflux ATPase. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[63]  D. Mengin-Lecreulx,et al.  An efflux transporter PbrA and a phosphatase PbrB cooperate in a lead‐resistance mechanism in bacteria , 2009, Molecular microbiology.

[64]  P. V. Bramhachari,et al.  Isolation and characterization of mucous exopolysaccharide (EPS) produced by Vibrio furnissii strain VB0S3. , 2007, Journal of microbiology and biotechnology.

[65]  K. Arunkumar,et al.  Bioremediation of chromium contaminated environments. , 2003, Indian journal of experimental biology.

[66]  E. Boyd,et al.  The Mercury Resistance Operon: From an Origin in a Geothermal Environment to an Efficient Detoxification Machine , 2012, Front. Microbio..

[67]  H. R. Dash,et al.  Heavy Metals and Hydrocarbons: Adverse Effects and Mechanism of Toxicity , 2014 .

[68]  Yun-Xing Wang,et al.  Cu(I)-mediated Allosteric Switching in a Copper-sensing Operon Repressor (CsoR)* , 2014, The Journal of Biological Chemistry.

[69]  Seung Hyun Kang,et al.  Bacteria Metabolically Engineered for Enhanced Phytochelatin Production and Cadmium Accumulation , 2007, Applied and Environmental Microbiology.

[70]  F. Morel,et al.  Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria , 2011, Proceedings of the National Academy of Sciences.

[71]  K. Pandiyan,et al.  Bioremediation of Heavy Metals from Soil and Aquatic Environment: An Overview of Principles and Criteria of Fundamental Processes , 2015 .

[72]  N. Imura,et al.  Role of hydrogen sulfide in mercury resistance determined by plasmid of Clostridium cochlearium T-2 , 1981, Archives of Microbiology.

[73]  G. Grass,et al.  Control of Expression of a Periplasmic Nickel Efflux Pump by Periplasmic Nickel Concentrations , 2005, Biometals.

[74]  Wanzhi. Wei,et al.  Bioremediation of heavy metals by growing hyperaccumulaor endophytic bacterium Bacillus sp. L14. , 2010, Bioresource technology.

[75]  T. Cavalier-smith.  Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. , 2005, Annals of botany.

[76]  K. Smith,et al.  Genetic Studies on Plasmid-Linked Cadmium Resistance in Staphylococcus aureus , 1972, Journal of bacteriology.

[77]  D. Cooksey,et al.  Induction of the copper resistance operon from Pseudomonas syringae , 1988, Journal of bacteriology.

[78]  K. Timmis,et al.  Bacteria designed for bioremediation. , 1999, Trends in biotechnology.

[79]  H. R. Dash,et al.  Bioremediation of inorganic mercury through volatilization and biosorption by transgenic Bacillus cereus BW-03(pPW-05) , 2015 .

[80]  G. Stewart,et al.  Cloning and Expression of cadD, a New Cadmium Resistance Gene of Staphylococcus aureus , 1999, Journal of bacteriology.

[81]  M. Naik,et al.  Lead-Enhanced Siderophore Production and Alteration in Cell Morphology in a Pb-Resistant Pseudomonas aeruginosa Strain 4EA , 2011, Current Microbiology.

[82]  V. de Lorenzo,et al.  Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. , 2002, FEMS microbiology reviews.

[83]  H. R. Dash,et al.  Bioremediation of mercury and the importance of bacterial mer genes , 2012 .

[84]  A. Müller,et al.  Linkage between Catecholate Siderophores and the Multicopper Oxidase CueO in Escherichia coli , 2004, Journal of bacteriology.

[85]  N. Ramaiah,et al.  Detoxification of Toxic Heavy Metals by Marine Bacteria Highly Resistant to Mercury , 2008, Marine Biotechnology.

[86]  A. Matin,et al.  Mechanism of chromate reduction by the Escherichia coli protein, NfsA, and the role of different chromate reductases in minimizing oxidative stress during chromate reduction. , 2004, Environmental microbiology.

[87]  Susan M. Miller,et al.  Bacterial mercury resistance from atoms to ecosystems. , 2003, FEMS microbiology reviews.

[88]  C. Bender,et al.  Indigenous plasmids in Pseudomonas syringae pv. tomato: conjugative transfer and role in copper resistance , 1986, Journal of bacteriology.

[89]  S. Kumari,et al.  Marine bacteria: potential candidates for enhanced bioremediation , 2012, Applied Microbiology and Biotechnology.

[90]  M. Aguilera,et al.  Biosorption of heavy metals by the exopolysaccharide produced by Paenibacillus jamilae , 2008 .

[91]  A. Paul,et al.  Microbial extracellular polymeric substances: central elements in heavy metal bioremediation , 2008, Indian Journal of Microbiology.

[92]  R. Maier,et al.  Impact of metals on the biodegradation of organic pollutants. , 2003, Environmental health perspectives.

[93]  S. Silver,et al.  Cadmium and manganese transport in Staphylococcus aureus membrane vesicles , 1982, Journal of bacteriology.

[94]  C. Lim,et al.  Copper Resistance Gene Homologs in Pathogenic and Saprophytic Bacterial Species from Tomato , 1990, Applied and environmental microbiology.

[95]  D. Taylor,et al.  Helicobacter pylori genes hpcopA and hpcopP constitute a cop operon involved in copper export. , 1996, FEMS microbiology letters.

[96]  D. Pieper,et al.  Engineering bacteria for bioremediation. , 2000, Current opinion in biotechnology.

[97]  P. Blum,et al.  Role of MerH in mercury resistance in the archaeon Sulfolobus solfataricus. , 2013, Microbiology.

[98]  V. de Lorenzo,et al.  Mini‐transposons in microbial ecology and environmental biotechnology , 1998, FEMS Microbiology Ecology.

[99]  M. Marahiel,et al.  Copper Acquisition Is Mediated by YcnJ and Regulated by YcnK and CsoR in Bacillus subtilis , 2009, Journal of bacteriology.

[100]  B. B,et al.  Potential of Mercury-Resistant Marine Bacteria for Detoxification of Chemicals of Environmental Concern , 2007 .

[101]  M. Pillay,et al.  Characterization and Structure Prediction of Partial Length Protein Sequences of pcoA, pcoR and chrB Genes from Heavy Metal Resistant Bacteria from the Klip River, South Africa , 2015, International journal of molecular sciences.

[102]  L. Giovannetti,et al.  Molecular mechanisms of Cr(VI) resistance in bacteria and fungi. , 2014, FEMS microbiology reviews.

[103]  J. Crowley,et al.  The siderophore yersiniabactin binds copper to protect pathogens during infection , 2012, Nature chemical biology.

[104]  A. Rosenzweig,et al.  Dual Pathways for Copper Uptake by Methanotrophic Bacteria* , 2011, The Journal of Biological Chemistry.

[105]  A. Osborn,et al.  Distribution, diversity and evolution of the bacterial mercury resistance (mer) operon. , 1997, FEMS microbiology reviews.

[106]  Y. L. Huang,et al.  Bioaccumulation of nickel from aqueous solutions by genetically engineered Escherichia coli. , 2003, Water research.

[107]  Jin-Town Wang,et al.  CadC regulates cad and tdc operons in response to gastrointestinal stresses and enhances intestinal colonization of Klebsiella pneumoniae. , 2010, The Journal of infectious diseases.

[108]  Ritesh Mishra,et al.  Reduction of Chromium-VI by Chromium Resistant Lactobacilli: A Prospective Bacterium for Bioremediation , 2012, Toxicology international.

[109]  N. Brown,et al.  Cloning and Functional Analysis of thepbr Lead Resistance Determinant of Ralstonia metallidurans CH34 , 2001, Journal of bacteriology.

[110]  T. Roane.  Lead Resistance in Two Bacterial Isolates from Heavy Metal–Contaminated Soils , 1999, Microbial Ecology.

[111]  M. Zhang,et al.  Molecular analysis of the copper-responsive CopRSCD of a pathogenic Pseudomonas fluorescens strain , 2009, The Journal of Microbiology.

[112]  中尾 光輝,et al.  KEGG(Kyoto Encyclopedia of Genes and Genomes)〔和文〕 (特集 ゲノム医学の現在と未来--基礎と臨床) -- (データベース) , 2000 .

[113]  Hauke Harms,et al.  Principles of microbial PAH-degradation in soil. , 2005, Environmental pollution.

[114]  S. Singh,et al.  Cuprous Oxidase Activity of CueO from Escherichia coli , 2004, Journal of bacteriology.

[115]  S. Hasnain,et al.  Hexavalent chromium reduction by bacteria from tannery effluent. , 2012, Journal of microbiology and biotechnology.

[116]  M. Mergeay,et al.  Regulation of the cnr Cobalt and Nickel Resistance Determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34 , 2000, Journal of bacteriology.

[117]  S. Bereswill,et al.  The Novel Helicobacter pylori CznABC Metal Efflux Pump Is Required for Cadmium, Zinc, and Nickel Resistance,Urease Modulation, and Gastric Colonization , 2006, Infection and Immunity.

[118]  Rudolf Amann,et al.  Fluorescence In Situ Hybridization and Catalyzed Reporter Deposition for the Identification of Marine Bacteria , 2002, Applied and Environmental Microbiology.

[119]  R. Moreno-Sánchez,et al.  Short-Chain Chromate Ion Transporter Proteins from Bacillus subtilis Confer Chromate Resistance in Escherichia coli , 2009, Journal of bacteriology.

[120]  M. Benedetti,et al.  Competitive Binding of Protons, Calcium, Cadmium, and Zinc to Isolated Cell Walls of a Gram-Positive Soil Bacterium , 1996 .

[121]  B. Volesky,et al.  Advances in the biosorption of heavy metals , 1998 .

[122]  H. Naser.  Assessment and management of heavy metal pollution in the marine environment of the Arabian Gulf: a review. , 2013, Marine pollution bulletin.

[123]  J. Ramos,et al.  Construction and behavior of biologically contained bacteria for environmental applications in bioremediation , 1995, Applied and environmental microbiology.

[124]  B. Volesky,et al.  Biosorption: a solution to pollution? , 2000, International microbiology : the official journal of the Spanish Society for Microbiology.

[125]  D. Daffonchio,et al.  Identification of molecular markers to follow up the bioremediation of sites contaminated with chlorinated compounds. , 2010, Methods in molecular biology.

[126]  Prasenjit Das,et al.  Nickel Bioremediation Potential of Bacillus thuringiensis KUNi1 and Some Environmental Factors in Nickel Removal , 2014 .

[127]  S. Silver,et al.  Bacterial transformations of and resistances to heavy metals. , 1984, Basic life sciences.

[128]  S. Kumari,et al.  Understanding molecular identification and polyphasic taxonomic approaches for genetic relatedness and phylogenetic relationships of microorganisms. , 2014, Journal of microbiological methods.

[129]  K. Minton,et al.  Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments , 2000, Nature Biotechnology.

[130]  N. Bhosle,et al.  Bacterial extracellular polymeric substance (EPS): a carrier of heavy metals in the marine food-chain. , 2006, Environment international.

[131]  S. Ravikumar,et al.  Biosorption and bio-kinetic studies of halobacterial strains against Ni2+, Al3+ and Hg2+ metal ions. , 2012, Bioresource technology.

[132]  N. Vats,et al.  Characterization of a copper-transport operon, copYAZ, from Streptococcus mutans. , 2001, Microbiology.

[133]  G. Gadd,et al.  Cadmium transport, resistance, and toxicity in bacteria, algae, and fungi. , 1986, Canadian journal of microbiology.

[134]  Hahn,et al.  Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. , 1999, FEMS microbiology ecology.

[135]  A. Matin,et al.  Purification to Homogeneity and Characterization of a Novel Pseudomonas putida Chromate Reductase , 2000, Applied and Environmental Microbiology.

[136]  I. Wagner-Döbler,et al.  Pilot plant for bioremediation of mercury-containing industrial wastewater , 2003, Applied Microbiology and Biotechnology.

[137]  M. Seeger,et al.  Characterization of the Metabolically Modified Heavy Metal-Resistant Cupriavidus metallidurans Strain MSR33 Generated for Mercury Bioremediation , 2011, PloS one.

[138]  D. Nies,et al.  New genes involved in chromate resistance in Ralstonia metallidurans strain CH34 , 2004, Archives of Microbiology.

[139]  Jie Liu,et al.  Metallothionein: an intracellular protein to protect against cadmium toxicity. , 1999, Annual review of pharmacology and toxicology.

[140]  Xiaohui Zhou,et al.  Plasmid-borne cadmium resistant determinants are associated with the susceptibility of Listeria monocytogenes to bacteriophage. , 2015, Microbiological research.

[141]  J. Pandey,et al.  Accessing microbial diversity for bioremediation and environmental restoration. , 2005, Trends in biotechnology.

[142]  H. Schlegel,et al.  Combined nickel-cobalt-cadmium resistance encoded by the ncc locus of Alcaligenes xylosoxidans 31A , 1994, Journal of bacteriology.

[143]  Alok Srivastava,et al.  Application of Monooxygenases in Dehalogenation, Desulphurization, Denitrification and Hydroxylation of Aromatic Compounds , 2010 .

[144]  A. G. Wedd,et al.  Reaction mechanisms of the multicopper oxidase CueO from Escherichia coli support its functional role as a cuprous oxidase. , 2010, Journal of the American Chemical Society.

[145]  M. Mergeay,et al.  Lead(II) resistance in Cupriavidus metallidurans CH34: interplay between plasmid and chromosomally-located functions , 2009, Antonie van Leeuwenhoek.

[146]  P. Gunasekaran,et al.  Extracellular synthesis and characterization of nickel oxide nanoparticles from Microbacterium sp. MRS-1 towards bioremediation of nickel electroplating industrial effluent. , 2014, Bioresource technology.

[147]  Dietrich H. Nies,et al.  Regulation of the cnr Cobalt and Nickel Resistance Determinant from Ralstonia sp. Strain CH34 , 2000, Journal of bacteriology.

[148]  K. Timmis,et al.  Microbial retention of mercury from waste streams in a laboratory column containing merA gene bacteria. , 1993, FEMS microbiology reviews.

[149]  P. Blum,et al.  Regulation of Mercury Resistance in the Crenarchaeote Sulfolobus solfataricus , 2006, Journal of bacteriology.

[150]  M. Kiyono,et al.  The merG Gene Product Is Involved in Phenylmercury Resistance in Pseudomonas Strain K-62 , 1999, Journal of bacteriology.

[151]  Z. Gorlenko,et al.  Tn5037, a Tn21-like Mercury Resistance transposon from Thiobacillus ferrooxidans , 2001, Russian Journal of Genetics.

[152]  R. Francisco,et al.  Chromium resistance strategies and toxicity: what makes Ochrobactrum tritici 5bvl1 a strain highly resistant , 2011, BioMetals.

[153]  C. Rensing,et al.  Molecular Analysis of the Copper-Transporting Efflux System CusCFBA of Escherichia coli , 2003, Journal of bacteriology.

[154]  Masa H. Sato,et al.  Bacterial heavy metal transporter MerC increases mercury accumulation in Arabidopsis thaliana , 2013 .

[155]  A. Matin,et al.  ChrR, a Soluble Quinone Reductase of Pseudomonas putida That Defends against H2O2* , 2005, Journal of Biological Chemistry.

[156]  S. Minakhina,et al.  Mercury resistance transposons of gram-negative environmental bacteria and their classification. , 2001, Research in microbiology.

[157]  M. Aumercier,et al.  Potentiation by salicylate and salicyl alcohol of cadmium toxicity and accumulation in Escherichia coli , 1990, Antimicrobial Agents and Chemotherapy.

[158]  L. Sahlman,et al.  1H NMR studies of the mercuric ion binding protein MerP: Sequential assignment, secondary structure and global fold of oxidized MerP , 1993, Journal of biomolecular NMR.

[159]  B. Mattiasson,et al.  Sulphate reducing bacteria to precipitate mercury after electrokinetic soil remediation , 2008 .

[160]  Oscar N. Ruiz,et al.  Characterization of mercury bioremediation by transgenic bacteria expressing metallothionein and polyphosphate kinase , 2011, BMC biotechnology.

[161]  A. Summers,et al.  Roles of the Tn21 merT, merP, and merC gene products in mercury resistance and mercury binding , 1992, Journal of bacteriology.