Advertisement

Applied Microbiology and Biotechnology

, Volume 100, Issue 7, pp 2967–2984 | Cite as

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

  • Surajit DasEmail author
  • Hirak R. Dash
  • Jaya Chakraborty
Mini-Review

Abstract

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.

Keywords

Bioremediation Metal resistant genes Bacterial diversity Gene manipulation Metal resistance 

Notes

Acknowledgments

Authors would like to acknowledge the authorities of NIT, Rourkela, for providing facilities. Financial supports received by S.D. through the research projects from the Department of Biotechnology, Ministry of Science and Technology, Government of India, on various aspects of microbial bioremediation of organic and inorganic contaminants is gratefully acknowledged.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Abdel-Monem MO, Al-Zubeiry AH, Al-Gheethi AA (2010) Biosorption of nickel by Pseudomonas cepacia 120S and Bacillus subtilis 117S. Water Sci Technol 61(12):2994–3007PubMedCrossRefGoogle Scholar
  2. Ackerley DF, Gonzalez CF, Keyhan M, Blake R, Matin A (2004) Mechanism of chromate reduction by the Escherichia coli protein, NfsA, and the role of different chromate reductases in minimizing oxidative stress during chromate reduction. Environ Microbiol 6:851–860PubMedCrossRefGoogle Scholar
  3. Albarracin VH, Avila AL, Amoroso MJ, Abate CM (2008) Copper removal ability by Streptomyces strains with dissimilar growth patterns and endowed with cupric reductase activity. FEMS Microbiol Lett 288:141–148PubMedCrossRefGoogle Scholar
  4. Arora PK, Srivastava A, Singh VP (2010) Application of monooxygenases in dehalogenation, desulphurization, denitrification and hydroxylation of aromatic compounds. J Bioremed Biodegrad 1:112. doi: 10.4172/2155-6199.1000112 CrossRefGoogle Scholar
  5. Balasubramanian R, Kenney GE, Rosenzweig AC (2011) Dual pathways for copper uptake by methanotrophic bacteria. J Biol Chem 286:37313–37319PubMedPubMedCentralCrossRefGoogle Scholar
  6. Barkay T, Wagner-Dobler I (2005) Microbial transformations of mercury: potentials, challenges, and achievements in controlling mercury toxicity in the environment. Adv Appl Microbiol 57(1):1–52PubMedCrossRefGoogle Scholar
  7. Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384PubMedCrossRefGoogle Scholar
  8. Batool R, Yrjala K, Hasnain S (2012) Hexavalent chromium reduction by bacteria from tannery effluent. J Microbiol Biotechnol 22:547–554PubMedCrossRefGoogle Scholar
  9. Bender CL, Cooksey DA (1986) Indigenous plasmids in Pseudomonas syringae pv. tomato: conjugative transfer and role in copper resistance. J Bacteriol 165:534–541PubMedPubMedCentralGoogle Scholar
  10. Bhaskar PV, Bhosle NB (2006) Bacterial extracellular polymeric substances (EPS) a carrier of heavy metals in the marine food-chain. Environ Int 32:192–198CrossRefGoogle Scholar
  11. Blindauer CA, Harrison MD, Robinson AK, Parkinson JA, Bowness PW, Sadler PJ, Robinson NJ (2002) Multiple bacteria encode metallothioneins and SmtA-like zinc fingers. Mol Microbiol 45(5):1421–1432PubMedCrossRefGoogle Scholar
  12. Bondarczuk K, Piotrowska-Seget Z (2013) Molecular basis of active copper resistance mechanisms in Gram-negative bacteria. Cell Biol Toxicol 29:397–405PubMedPubMedCentralCrossRefGoogle Scholar
  13. Borremans B, Hobman JL, Provoost A, Brown NL, van Der Lelie D (2001) Cloning and functional analysis of the pbr lead resistance determinant of Ralstonia metallidurans CH34. J Bacteriol 183:5651–5658PubMedPubMedCentralCrossRefGoogle Scholar
  14. Boyd ES, Barkay T (2012) The mercury resistance operon: from an origin in a geothermal environment to an efficient detoxification machine. Front Microbiol 3. doi: 10.3389/fmicb.2012.00349
  15. Bramhachari PV, Kavi Kishor PB, Ramadevi R, Kumar R, Rao BR, Dubey SK (2007) Isolation and characterization of mucous exopolysaccharide produced by Vibrio furnissii VB0S3. J Microbiol Biotechnol 17:44–51PubMedGoogle Scholar
  16. Branco R, Chung AP, Johnston T, Gurel V, Morais P, Zhitkovich A (2008) The chromate-inducible chrBACF operon from the transposable element TnOtChr confers resistance to chromium (VI) and superoxide. J Bacteriol 190(21):6996–7003PubMedPubMedCentralCrossRefGoogle Scholar
  17. Brim H, McFarlan SC, Fredrickson JK, Minton KW, Zhai M, Wackett LP, Daly MJ (2000) Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments. Nat Biotechnol 18:85–90PubMedCrossRefGoogle Scholar
  18. Brim H, Venkateswaran A, Kostandarithes HM, Fredrickson JK, Daly MJ (2003) Engineering Deinococcus geothermalis for bioremediation of high-temperature radioactive waste environments. Appl Environ Microbiol 69:4575–4582PubMedPubMedCentralCrossRefGoogle Scholar
  19. Brunke M, Deckwer WD, Frischmuth A, Horn JM, Lünsdorf H, Rhode M, Röhricht M, Timmis KN, Weppen P (1993) Microbial retention of mercury from waste streams in a laboratory column containing merA gene bacteria. FEMS Microbiol Rev 11(1–3):145–152PubMedCrossRefGoogle Scholar
  20. Cervantes C, Campos-García J (2007) Reduction and efflux of chromate by bacteria. In: molecular microbiology of heavy metals. Springer Berlin, Heidelberg, pp. 407–419CrossRefGoogle Scholar
  21. Chakraborty J, Das S (2014) Characterization and cadmium-resistant gene expression of biofilm-forming marine bacterium Pseudomonas aeruginosa JP-11. Environ Sci Pollut Res. doi: 10.1007/s11356-014-3308-7 Google Scholar
  22. Chang FM, Coyne HJ, Cubillas C, Vinuesa P, Fang X, Ma Z, Ma D, Helmann JD, García-de los Santos A, Wang YX, Dann CE3rd, Giedroc DP (2014) Cu(I)-mediated allosteric switching in a copper-sensing operon repressor (CsoR). J Biol Chem 289(27):19204–19217Google Scholar
  23. Chaouni LBA, Etienne J, Greenland T, Vandenesch F (1996) Nucleic acid sequence and affiliation of pLUG10, a novel cadmium resistance plasmid from Staphylococcus lugdunensis. Plasmid 36:1–8PubMedCrossRefGoogle Scholar
  24. Chaturvedi R, Archana G (2014) Cytosolic expression of synthetic phytochelatin and bacterial metallothionein genes in Deinococcus radiodurans R1 for enhanced tolerance and bioaccumulation of cadmium. Biometals 27(3):471–482PubMedCrossRefGoogle Scholar
  25. Chaturvedi KS, Hung CS, Crowley JR, Stapleton AE, Henderson JP (2012) The siderophore yersiniabactin binds copper to protect pathogens during infection. Nat Chem Biol 8:731–736PubMedPubMedCentralCrossRefGoogle Scholar
  26. Chaturvedi KS, Hung CS, Giblin DE, Urushidani S, Austin AM, Dinauer MC, Henderson JP (2014) Cupric yersiniabactin is a virulence-associated superoxide dismutase mimic. ACS Chem Biol 9:551–561PubMedPubMedCentralCrossRefGoogle Scholar
  27. Chihomvu P, Stegmann P, Pillay M (2015) 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. Int J Mol Sci 16:7352–7374PubMedPubMedCentralCrossRefGoogle Scholar
  28. Chillappagari S, Miethke M, Trip H, Kuipers OP, Marahiel MA (2009) Copper acquisition is mediated by YcnJ and regulated by YcnK and CsoR in Bacillus subtilis. J Bacteriol 191:2362–2370PubMedPubMedCentralCrossRefGoogle Scholar
  29. Cooksey DA, Azad HR, Cha JS, Lim CK (1990) Copper resistance gene homologs in pathogenic and saprophytic bacterial species from tomato. Appl Environ Microbiol 56:431–435PubMedPubMedCentralGoogle Scholar
  30. Crupper SS, Worrell V, Stewart GC, Iandolo JJ (1999) Cloning and expression of cadD, a new cadmium resistance gene of Staphylococcus aureus. J Bacteriol 181:4071–4075PubMedPubMedCentralGoogle Scholar
  31. Das S (2014) Microbial biodegradation and bioremediation. Elsevier, USA, p. 634Google Scholar
  32. Das S, Raj R, Mangwani N, Dash HR, Chakraborty J (2014a) Heavy metals and hydrocarbons: adverse effects and mechanism of toxicity. In: Das S (ed) Microbial Biodegradation and Bioremediation. Elsevier, USA, pp. 23–54CrossRefGoogle Scholar
  33. Das S, Dash HR, Mangwani N, Chakraborty J, Kumari S (2014b) Understanding molecular identification and polyphasic taxonomic approaches for genetic relatedness and phylogenetic relationships of microorganisms. J Microbiol Meth 103:80–100CrossRefGoogle Scholar
  34. Das P, Sinha S, Mukherjee SK (2014c) Nickel bioremediation potential of Bacillus thuringiensis KUNi1 and some environmental factors in nickel removal. Bioremediation J 18(2):169–177CrossRefGoogle Scholar
  35. Dash HR, Das S (2012) Bioremediation of mercury and the importance of bacterial mer genes. Int Biodet Biodeg 75:207–213CrossRefGoogle Scholar
  36. Dash HR, Das S (2015) Enhanced bioremediation of inorganic mercury through simultaneous volatilization and biosorption by transgenic marine bacterium Bacillus cereus BW-03(pPW-05). Int Biodeterior Biodegrad 103:179–185CrossRefGoogle Scholar
  37. Dash HR, Mangwani N, Chakraborty J, Kumari S, Das S (2013) Marine bacteria: potential candidates for enhanced bioremediation. Appl Microbiol Biotechnol 97:561–571PubMedCrossRefGoogle Scholar
  38. Dash HR, Mangwani N, Das S (2014) Characterization and potential application in mercury bioremediation of highly mercury-resistant marine bacterium Bacillus thuringiensis PW-05. Environ Sci Pollut Res 21(4):2642–2653CrossRefGoogle Scholar
  39. De J, Ramaiah N, Bhosle NB, Garg A, Vardanyan L, Nagle VL, Fukami K (2007) Potential of mercury resistant marine bacteria for detoxification of chemicals of environmental concern. Microbes Environ 22:336–345CrossRefGoogle Scholar
  40. De J, Ramaiah N, Vardanyan L (2008) Detoxification of toxic heavy metals by marine bacteria highly resistant to mercury. Mar Biotechnol 10:471–477PubMedCrossRefGoogle Scholar
  41. Deng X, Li QB, Lu YH, Sun DH, Huang YL, Chen XR (2003) Bioaccumulation of nickel from aqueous solutions by genetically engineered Escherichia coli. Water Res 37(10):2505–2511PubMedCrossRefGoogle Scholar
  42. Diaz-Magana A, Aguilar-Barajas E, Moreno-Sánchez R, Ramírez-Díaz MI, Riveros-Rosas H, Vargas E, Cervantes C (2009) Short-chain chromate ion transporter proteins from Bacillus subtilis confer chromate resistance in Escherichia coli. J Bacteriol 191:5441–5445PubMedPubMedCentralCrossRefGoogle Scholar
  43. Dixit R, Malaviya D, Pandiyan K, Singh UB, Sahu A, Shukla R, Singh BP, Rai JP, Sharma PK, Lade H, Paul D (2015) Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustainability 7(2):2189–2212CrossRefGoogle Scholar
  44. Djoko KY, Chong LX, Wedd AG, Xiao Z (2010) Reaction mechanisms of the multicopper oxidase CueO from Escherichia coli support its functional role as a cuprous oxidase. J Am Chem Soc 132:2005–2015PubMedCrossRefGoogle Scholar
  45. Duprey A, Chansavang V, Frémion F, Gonthier C, Louis Y, Lejeune P, Dorel C (2014) “NiCo Buster”: engineering E. coli for fast and efficient capture of cobalt and nickel. J Biol Eng 8(1):1–11CrossRefGoogle Scholar
  46. Eriksson PO, Sahlman L (1993) 1H NMR studies of the mercuric ion binding protein MerP: sequential assignment, secondary structure and global fold of oxidized MerP. J Biomol NMR 3:613–626PubMedCrossRefGoogle Scholar
  47. Franke S, Grass G, Rensing C, Nies DH (2003) Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J Bacteriol 185(13):3804–3812PubMedPubMedCentralCrossRefGoogle Scholar
  48. Ge Z, Taylor DE (1996) Helicobacter pylori genes hpcopA and hpcopP constitute a cop operon involved in copper export. FEMS Microbiol Lett 145:181–188PubMedCrossRefGoogle Scholar
  49. Gee AR, Dudeney AWL (1998) Adsorption and crystallization of gold at biological surfaces. In PR Norris, DP Kelly (Eds). Proceedings of the international symposium on Biohydrometallurgy (pp 437–451)Google Scholar
  50. Golby S, Ceri H, Marques LLR, Turner RJ (2014) Mixed-species biofilms cultured from an oil sand tailings pond can biomineralize metals. Microb Ecol 68:70–80PubMedCrossRefGoogle Scholar
  51. Gonzalez CF, Ackerley DF, Lynch SV, Matin A (2005) ChrR, a soluble quinone reductase of Pseudomonas putida that defends against H2O2. J Biol Chem 280:22590–22595PubMedCrossRefGoogle Scholar
  52. Grass G, Große C, Nies DH (2000) Regulation of the cnr cobalt and nickel resistance determinant from Ralstonia sp. strain CH34. J Bacteriol 182:1390–1398PubMedPubMedCentralCrossRefGoogle Scholar
  53. Grass G, Thakali K, Klebba PE, Thieme D, Muller A, Wildner GF, Rensing C (2004) Linkage between catecholate siderophores and the multicopper oxidase CueO in Escherichia coli. J Bacteriol 186:5826–5833PubMedPubMedCentralCrossRefGoogle Scholar
  54. Grass G, Fricke B, Nies DH (2005) Control of expression of a periplasmic nickel efflux pump by periplasmic nickel concentrations. Biometals 18:437–448PubMedCrossRefGoogle Scholar
  55. Guo H, Luoa S, Chen L, Xiao X, Xi Q, Wei W, Zeng G, Liu C, Wan Y, Chen J, He Y (2010) Bioremediation of heavy metals by growing hyperaccumulaor endophytic bacterium Bacillus sp. L14. Bioresour Technol 101:8599–8606PubMedCrossRefGoogle Scholar
  56. Hakansson T, Suer P, Mattiasson B, Allard B (2008) Sulphate reducing bacteria to precipitate mercury after electrokinetic soil remediation. Int J Environ Sci Technol 5(2):267–274CrossRefGoogle Scholar
  57. Hamlett NV, Landale EC, Davis BH, Summers AO (1992) Roles of the Tn21 merT, merP, and merC gene products in mercury resistance and mercury binding. J Bacteriol 174(20):6377–6385PubMedPubMedCentralGoogle Scholar
  58. Henne KL, Nakatsu CH, Thompson DK, Konopka AE (2009) High-level chromate resistance in Arthrobacter sp. strain FB24 requires previously uncharacterized accessory genes. BMC Microbiol 9:199PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hinojosa BM, Garcia-Ruiz R, Carreira JA (2010) Utilizing microbial community structure and function to evaluate the health of heavy metal polluted soils. In Soil Heavy Metals by Sherameti I, Varma A. Chapter 9Google Scholar
  60. Hsieh PF, Lin HH, Lin TL, Wang JT (2010) CadC regulates cad and tdc operons in response to gastrointestinal stresses and enhances intestinal colonization of Klebsiella pneumoniae. J Infect Dis 202:52–64PubMedCrossRefGoogle Scholar
  61. Hu YH, Wang HL, Zhang M, Sun L (2009) Molecular analysis of the copper-responsive CopRSCD of a pathogenic Pseudomonas fluorescens strain. J Microbiol 47:277–286PubMedCrossRefGoogle Scholar
  62. Hynninen A, Touze T, Pitkänen L, Mengin-Lecreulx D, Virta M (2009) An efflux transporter PbrA and a phosphatase PbrB cooperate in a lead-resistance mechanism in bacteria. Mol Microbiol 74:384–394PubMedCrossRefGoogle Scholar
  63. Jarosławiecka A, Piotrowska-Seget Z (2014) Lead resistance in micro-organisms. Microbiology 160:12–25PubMedCrossRefGoogle Scholar
  64. Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:71–84PubMedCrossRefGoogle Scholar
  65. Juhnke S, Peitzsch N, Hübener N, Grobe C, Nies DH (2002) New genes involved in chromate resistance in Ralstonia metallidurans strain CH34. Arch Microbiol 179:15–25PubMedCrossRefGoogle Scholar
  66. Kalyaeva ES, Kholodii GY, Bass IA, Gorlenko ZM, Yurieva OV, Nikiforov VG (2001) Tn5037, a Tn21-like mercury resistance transposon from Thiobacillus ferrooxidans. Rus J Gen 37:972–975CrossRefGoogle Scholar
  67. Kamaludeen SPB, Arunkumar KR, Avudainayagam SA, Ramasamy K (2003) Bioremediation of chromium contaminated environments. Indian J Exp Biol 41:972–985PubMedGoogle Scholar
  68. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30Google Scholar
  69. Kang SH, Singh S, Kim JY, Lee W, Mulchandani A, Chen W (2007) Bacteria metabolically engineered for enhanced phytochelatin production and cadmium accumulation. Appl Environ Microbiol 73:6317–6320Google Scholar
  70. Karp PD, Ouzounis CA, Moore-Kochlacs C, Goldovsky L, Kaipa P, Ahrén D, Ópez-Bigas N (2005) Expansion of the BioCyc collection of pathway/genome databases to 160 genomes. Nucleic Acids Res 33:6083–6089PubMedPubMedCentralCrossRefGoogle Scholar
  71. Kermani AJN, Ghasemi MF, Khosravan A, Farahmand A, Shakibaie MR (2010) Cadmium bioremediation by metal-resistant mutated bacteria isolated from active sludge of industrial effluent. Ira J Environ Health Sci Eng 7(4):279–286Google Scholar
  72. Khan F, Sajid M, Cameotra SS (2013) In silico approach for the bioremediation of toxic pollutants. J Pet Environ Biotechnol 4:2CrossRefGoogle Scholar
  73. Khan Z, Nisar MA, Hussain SZ, Arshad MN, Rehman A (2015) Cadmium resistance mechanism in Escherichia coli P4 and its potential use to bioremediate environmental cadmium. Appl Microbiol Biotechnol 99(24):10745–10757PubMedCrossRefGoogle Scholar
  74. Kiyono M, Pan-Hou H (1999) The merG gene product is involved in phenylmercury resistance in Pseudomonas strain K-62. J Bacteriol 181:726–730PubMedPubMedCentralGoogle Scholar
  75. Kiyono M, Oka Y, Sone Y, Nakamura R, Sato MH, Sakabe K, Pan-Hou H (2013) Bacterial heavy metal transporter MerC increases mercury accumulation in Arabidopsis thaliana. Biochem Engin J 71:19–24CrossRefGoogle Scholar
  76. Klaassen CD, Liu SCJ (1999) Metallothionein: an intracellular protein to protect against cadmium toxicity. Ann Rev Pharmacol Toxicol 39:267–294CrossRefGoogle Scholar
  77. Kornberg A (1995) Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J Bacteriol 177:491–496PubMedPubMedCentralGoogle Scholar
  78. Kratchovil D, Volesky B (1998) Advances in the biosorption of heavy metals. Trends Biotechnol 16:291–300CrossRefGoogle Scholar
  79. Letunic I, Copley RR, Pils B, Pinkert S, Schultz J, Bork P (2006) SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 34:D257–D260PubMedPubMedCentralCrossRefGoogle Scholar
  80. Lorenzo V, Herrero M, Sánchez JM, Timmis KN (1998) Mini-transposons in microbial ecology and environmental biotechnology. FEMS Microbiol Ecol 27:211–224CrossRefGoogle Scholar
  81. Lovley DR, Coates JD (1997) Bioremediation of metal contamination. Curr Opin Biotechnol 8:285–289PubMedCrossRefGoogle Scholar
  82. Macomber L, Imlay JA (2009) The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci U S A 106:8344–8349PubMedPubMedCentralCrossRefGoogle Scholar
  83. Marzorati M, Balloi A, De Ferra F, Daffonchio D (2010) Identification of molecular markers to follow up the bioremediation of sites contaminated with chlorinated compounds. Methods Mol Biol 668:219–134PubMedCrossRefGoogle Scholar
  84. Mellano MA, Cooksey DA (1988) Induction of the copper resistance operon from Pseudomonas syringae. J Bacteriol 170:4399–4401PubMedPubMedCentralGoogle Scholar
  85. Mindlin S, Kholodii G, Gorlenko Z, Minakhina S, Minakhin L, Kalyaeva E, Nikiforov V (2001) Mercury resistance transposons of gram-negative environmental bacteria and their classification. Res Microbiol 152:811–822PubMedCrossRefGoogle Scholar
  86. Mishra R, Sinha V, Kannan A, Upreti RK (2012) Reduction of chromium-VI by chromium resistant Lactobacilli: a prospective bacterium for bioremediation. Toxicol Int 19:25–30PubMedPubMedCentralCrossRefGoogle Scholar
  87. Monchy S, Benotmane MA, Janssen P, Vallaeys T, Taghavi S, van der Lelie D, Mergeay M (2007) Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans are specialized in the maximal viable response to heavy metals. J Bacteriol 189(20):7417–7425PubMedPubMedCentralCrossRefGoogle Scholar
  88. Moore MJ, Distefano MD, Zydowsky LD, Cummings RT, Walsh CT (1990) Organomercurial lyase and mercuric ion reductase: nature’s mercury detoxification catalysts. Acc Chem Res 23:301–308CrossRefGoogle Scholar
  89. Morais PV, Branco R, Francisco R (2011) Chromium resistance strategies and toxicity: what makes Ochrobactrum tritici 5bvl1 a strain highly resistant. Biometals 24:401–410PubMedCrossRefGoogle Scholar
  90. Morillo JA, Garcia-Ribera R, Quesada T, Aguilera M, Ramos-Cormenzana A, Monteoliva-Sanchez M (2008) Biosorption of heavy metals by the exopolysaccharide produced by Paenibacillus jamilae. World J Microbiol Biotechnol 24:2699–2704CrossRefGoogle Scholar
  91. Munson GP, Lam DL, Outten FW, O’Halloran TV (2000) Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. J Bacteriol 182:5864–5871PubMedPubMedCentralCrossRefGoogle Scholar
  92. Naik MM, Dubey SK (2011) Lead-enhanced siderophore production and alteration in cell morphology in a Pb-resistant Pseudomonas aeruginosa strain 4EA. Curr Microbiol 62:409–414PubMedCrossRefGoogle Scholar
  93. Naik MM, Pandey A, Dubey SK (2012a) Pseudomonas aeruginosa strain WI-1 from Mandovi estuary possesses metallothionein to alleviate lead toxicity and promotes plant growth. Ecotoxicol Environ Safety 79:129–133PubMedCrossRefGoogle Scholar
  94. Naik MM, Shamim K, Dubey SK (2012b) Biological characterization of lead resistant bacteria to explore role of bacterial metallothioneinin lead resistance. Curr Sci 103:1–3Google Scholar
  95. Nascimento AM, Chartone-Souza E (2003) Operon mer: bacterial resistance to mercury and potential for bioremediation of contaminated environments. Gen Mol Res 2(1):92–101Google Scholar
  96. Naser HA (2013) Assessment and management of heavy metal pollution in the marine environment of the Arabian Gulf: a review. Mar Pollut Bull 72:6–13PubMedCrossRefGoogle Scholar
  97. Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339PubMedCrossRefGoogle Scholar
  98. Nies DH, Koch S, Wachi S, Peitzsch N, Saier MH (1998) CHR, a novel family of prokaryotic proton motive force-driven transporters probably containing chromate/sulfate antiporters. J Bacteriol 180:5799–5802PubMedPubMedCentralGoogle Scholar
  99. Niti C, Sunita S, Kamlesh K, Rakesh K (2013) Bioremediation: An emerging technology for remediation of pesticides. Res J Chem Environ 17:88–105Google Scholar
  100. Nucifora G, Chu L, Misra TK, Silver S (1989) Cadmium resistance from Staphylococcus aureus plasmid pI258 cadA gene results from a cadmium-efflux ATPase. Proc Nat Acad Sci 86:3544–3548PubMedPubMedCentralCrossRefGoogle Scholar
  101. Obenauer JC, Cantley LC, Yaffe MB (2003) Scansite 2.0: proteome-wide prediction of cell signalling interactions using short sequence motifs. Nucleic Acids Res 31:3635–3641PubMedPubMedCentralCrossRefGoogle Scholar
  102. Osborn AM, Bruce KD, Strike P, Ritchie DA (1997) Distribution, diversity and evolution of the bacterial mercury resistance (mer) operon. FEMS Microbiol Rev 19:239–262PubMedCrossRefGoogle Scholar
  103. Pal A, Paul AK (2008) Microbial extracellular polymeric substances: central elements in heavy metal bioremediation. Indian J Microbiol 48:49–64PubMedPubMedCentralCrossRefGoogle Scholar
  104. Pan-Hou HS, Imura N (1981) Role of hydrogen sulfide in mercury resistance determined by plasmid of Clostridium cochlearium T-2. Arch Microbiol 129(1):49–52PubMedCrossRefGoogle Scholar
  105. Pan-Hou H, Kiyono M, Omura T, Endo G (2002) Polyphosphate produced in recombinant Escherichia coli confers mercury resistance. FEMS Microbiol Lett 207:159–164PubMedCrossRefGoogle Scholar
  106. Park CH, Keyhan M, Wielinga B, Fendorf S, Matin A (2000) Purification to homogeneity and characterization of a novel Pseudomonas putida chromate reductase. Appl Environ Microbiol 66:1788–1795PubMedPubMedCentralCrossRefGoogle Scholar
  107. Park JH, Bolan N, Meghraj M, Naidu N (2011) Concomitant rock phosphate dissolution and lead immobilization by phosphate solubilising bacteria (Enterobacter sp.). J Environ Manag 92:1115–1120CrossRefGoogle Scholar
  108. Patra RC, Malik S, Beer M, Megharaj M, Naidu R (2010) Molecular characterization of chromium (VI) reducing potential in Gram positive bacteria isolated from contaminated sites. Soil Biol Biochem 42(10):1857–1863CrossRefGoogle Scholar
  109. Paul D, Pandey G, Pandey J, Jain RK (2005) Accessing microbial diversity for bioremediation and environmental restoration. Trends Biotechnol 23:135–142PubMedCrossRefGoogle Scholar
  110. Pernthaler A, Pernthaler J, Amann R (2002) Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68:3094–3101PubMedPubMedCentralCrossRefGoogle Scholar
  111. Perry RD, Silver S (1982) Cadmium and manganese transport in Staphylococcus aureus membrane vesicles. J Bacteriol 150:973–976PubMedPubMedCentralGoogle Scholar
  112. Pieper DH, Reineke W (2000) Engineering bacteria for bioremediation. Curr Opin Biotechnol 11:262–270PubMedCrossRefGoogle Scholar
  113. Plette AC, Benedetti MF, van Riemsdijk WH (1996) Competitive binding of protons, calcium, cadmium, and zinc to isolated cell walls of a gram-positive soil bacterium. Environ Sci Technol 30(6):1902–1910CrossRefGoogle Scholar
  114. Raj R, Dalei K, Chakraborty J, Das S (2016) Extracellular polymeric substances of a marine bacterium mediated synthesis of CdS nanoparticles for removal of cadmium from aqueous solution. J Colloid Interf Sci 462:166–175CrossRefGoogle Scholar
  115. Ravel J, Diruggiero J, Robb FT, Hill RT (2000) Cloning and sequence analysis of the mercury resistance operon of Streptomyces sp. strain CHR28 reveals a novel putative second regulatory gene. J Bacteriol 182:2345–2349PubMedPubMedCentralCrossRefGoogle Scholar
  116. Rebello RCL, Gomes KM, Duarte RS, Rachid CTCC, Rosado AS, Regua-Mangia AH (2013) Diversity of mercury resistant Escherichia coli strains isolated from aquatic systems in Rio de Janeiro. Brazil Int J Biodiv. doi: 10.1155/2013/265356 Google Scholar
  117. Roane TM (1999) Lead resistance in two bacterial isolates from heavy metal-contaminated soils. Microbial Ecol 37:218–224CrossRefGoogle Scholar
  118. Roane TM, Josephson KL, Pepper IL (2001) Dual-bioaugmentation strategy to enhance remediation of cocontaminated soil. Appl Environ Microbiol 67(7):3208–3215PubMedPubMedCentralCrossRefGoogle Scholar
  119. Robinson NJ, Gupta A, Fordham-Skelton AP, Croy RRD, Whitton BA, Huckle JW (1990) Prokaryotic metallothionein gene characterization and expression: chromosome crawling by ligation-mediated PCR. Proc R Soc London B 242:241–247CrossRefGoogle Scholar
  120. Rodrigue A, Effantin G, Mandrand-Berthelot MA (2005) Identification of rcnA (yohM), a nickel and cobalt resistance gene in Escherichia coli. J Bacteriol 187:2912–2916PubMedPubMedCentralCrossRefGoogle Scholar
  121. Rojas LA, Yáñez C, González M, Lobos S, Smalla K, Seeger M (2011) Characterization of the metabolically modified heavy metal-resistant Cupriavidus metallidurans strain MSR33 generated for mercury bioremediation. PLoS one 6:e17555PubMedPubMedCentralCrossRefGoogle Scholar
  122. Ronchel MC, Ramos C, Jensen LB, Molin S, Ramos JL (1995) Construction and behaviour of biologically contained bacteria for environmental adaptations in bioremediation. Appl Environ Microbiol 61:2990–2994PubMedPubMedCentralGoogle Scholar
  123. Rosner JL, Aumercier M (1990) Potentiation by salicylate and salicyl alcohol of cadmium toxicity and accumulation in Escherichia coli. Appl Environ Microbiol 34:2402–2406Google Scholar
  124. Ruiz ON, Alvarez D, Gonzalez-Ruiz G, Torres C (2011) Characterization of mercury bioremediation by transgenic bacteria expressing metallothionein and polyphosphate kinase. BMC Biotechnol 11:82PubMedPubMedCentralCrossRefGoogle Scholar
  125. Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L, Avison MB, Berg G, van der Lelie D, Dow JM (2009) The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 7:514–525PubMedCrossRefGoogle Scholar
  126. Sandaa RA, Torsvik V, Enger O, Daae FL, Castberg T, Hahn D (1999) Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. FEMS Microbiol Ecol 30:237–251PubMedCrossRefGoogle Scholar
  127. Sandrin TR, Maier RM (2003) Impact of metals on the biodegradation of organic pollutants. Environ Health Perspect 111(8):1093PubMedPubMedCentralCrossRefGoogle Scholar
  128. Sasaki Y, Hayakawa T, Inoue C, Miyazaki A, Silver S, Kusano T (2006) Generation of mercury-hyperaccumulating plants through transgenic expression of the bacterial mercury membrane transport protein MerC. Transgen Res 15:615–625CrossRefGoogle Scholar
  129. Sathyavathi S, Manjula A, Rajendhran J, Gunasekaran P (2014) Extracellular synthesis and characterization of nickel oxide nanoparticles from Microbacterium sp. MRS-1 towards bioremediation of nickel electroplating industrial effluent. Bioresour Technol 165:270–273PubMedCrossRefGoogle Scholar
  130. Schaefer JK, Rocks SS, Zheng W, Liang L, Gu B, Morel FMM (2011) Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria. Proc Nat Acad Sci USA 108:8714–8719PubMedPubMedCentralCrossRefGoogle Scholar
  131. Schelert J, Drozda M, Dixit V, Dillman A, Blum P (2006) Regulation of mercury resistance in the crenarchaeote Sulfolobus solfataricus. J Bacteriol 188:7141–7150PubMedPubMedCentralCrossRefGoogle Scholar
  132. Schelert J, Rudrappa D, Johnson T, Blum P (2013) Role of MerH in mercury resistance in the archaeon Sulfolobus solfataricus. Microbiol 159:1198–1208CrossRefGoogle Scholar
  133. Schmidt T, Schlegel HG (1994) Combined nickel-cobalt-cadmium resistance encoded by the ncc locus of Alcaligenes xylosoxidans 31A. J Bacteriol 176:7045-7054Google Scholar
  134. Schneiker S, Keller M, Dröge M, Lanka E, Pühler A, Selbitschka W (2001) 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. Nuc Acids Res 29:5169–5181CrossRefGoogle Scholar
  135. Schue M, Dover LG, Besra GS, Parkhill J, Brown NL (2009) Sequence and analysis of a plasmid-encoded mercury resistance operon from Mycobacterium marinum identifies MerH, a new mercuric ion transporter. J Bacteriol 191:439–444PubMedPubMedCentralCrossRefGoogle Scholar
  136. Silver S, Misra TK (1984) Bacterial transformations of and resistances to heavy metals. In: Genetic control of environmental pollutants. Springer USA, pp. 23–46Google Scholar
  137. Silver S, Phung LT (2013) Bacterial mercury resistance proteins. Encyclopedia of Metalloproteins 209-217Google Scholar
  138. Singh SK, Grass G, Rensing C, Montfort WR (2004) Cuprous oxidase activity of CueO from Escherichia coli. J Bacteriol 86:7815–7817CrossRefGoogle Scholar
  139. Smith TC (2005) Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Ann Bot 95:147–175CrossRefGoogle Scholar
  140. Smith K, Novick RP (1972) Genetic studies on plasmid-linked cadmium resistance in Staphylococcus aureus. J Bacteriol 112:761–772PubMedPubMedCentralGoogle Scholar
  141. Stahler FN, Odenbreit S, Haas R, Wilrich J, Van Vliet AH, Kusters JG, Kist M, Bereswill S (2006) The novel Helicobacter pylori CznABC metal efflux pump is required for cadmium, zinc, and nickel resistance, urease modulation, and gastric colonization. Infect Immun 74:3845–3852Google Scholar
  142. Taghavi S, Lesaulnier C, Monchy S, Wattiez R, Mergeay M, van der Lelie D (2009) Lead(II) resistance in Cupriavidus metallidurans CH34: interplay between plasmid and chromosomally-located functions. Antonie Van Leeuwenhoek 96:171–182PubMedCrossRefGoogle Scholar
  143. Tebo BM, Obraztova AY (1998) Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors. FEMS Microbiol Lett 162:193–198CrossRefGoogle Scholar
  144. Tetaz TJ, Luke RK (1983) Plasmid-controlled resistance to copper in Escherichia coli. J Bacteriol 154:1263–1268PubMedPubMedCentralGoogle Scholar
  145. Tibazarwa C, Wuertz S, Mergeay M, Wyns L, van Der Lelie D (2000) Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34. J Bacteriol 182(5):1399–1409PubMedPubMedCentralCrossRefGoogle Scholar
  146. Timmis KN, Pieper DH (1999) Bacteria designed for bioremediation. Trends Biotechnol 17:201–204CrossRefGoogle Scholar
  147. Trepreau J, de Rosny E, Duboc C, Sarret G, Petit-Hartlein I, Maillard AP, Covès J (2011) Spectroscopic characterization of the metal-binding sites in the periplasmic metal-sensor domain of CnrX from Cupriavidus metallidurans CH34. Biochem 50:9036–9045CrossRefGoogle Scholar
  148. Trevors JT, Stratton GW, Gadd GM (1986) Cadmium transport, resistance, and toxicity in bacteria, algae, and fungi. Can J Microbiol 32:447–464PubMedCrossRefGoogle Scholar
  149. Valls M, de Lorenzo V (2002) Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol Rev 26:327–338PubMedCrossRefGoogle Scholar
  150. Vargas-García MC, López MJ, Suárez-Estrella F, Moreno J (2012) Compost as a source of microbial isolates for the bioremediation of heavy metals: In vitro selection. Sci Total Environ 431:62–67CrossRefGoogle Scholar
  151. Vats N, Lee SF (2001) Characterization of a copper-transport operon, copYAZ, from Streptococcus mutans. Microbiol 147:653–662CrossRefGoogle Scholar
  152. Vieira RH, Volesky B (2010) Biosorption: a solution to pollution? Int Microbiol 3:17–24Google Scholar
  153. Vijayaraghavan K, Yun YS (2008) Bacterial biosorbents and biosorption. Biotechnol Adv 26:266–291PubMedCrossRefGoogle Scholar
  154. Viti C, Marchi E, Decorosi F, Giovannetti L (2013) Molecular mechanisms of Cr (VI) resistance in bacteria and fungi. FEMS Microbiol Rev 38:633–659PubMedCrossRefGoogle Scholar
  155. Von Mering C, Jensen CJ, Kuhn M, Chaffron S, Doerks M, Krüger B, Bork P (2007) STRING 7-recent developments in the integration and prediction of protein interactions. Nucleic Acids Res 35:D358–D362CrossRefGoogle Scholar
  156. von Rozycki T, Nies DH (2009) Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Antonie Van Leeuwenhoek 96(2):115–139CrossRefGoogle Scholar
  157. Wagner-Dobler I (2003) Pilot plant for bioremediation of mercury-containing industrial wastewater. Appl Microbiol Biotechnol 62(2–3):124–133PubMedCrossRefGoogle Scholar
  158. Williams GP, Gnanadesigan M, Ravikumar S (2012) Biosorption and bio-kinetic studies of halobacterial strains against Ni2+, Al3+ and Hg2+ metal ions. Bioresour Technol 107:526–529PubMedCrossRefGoogle Scholar
  159. Wu CH, Wood TK, Mulchandani A, Chen W (2006) Engineering plant-microbe symbiosis for rhizoremediation of heavy metals. Appl Environmental Microbiol 72:1129–1134Google Scholar
  160. Wunderli-Ye H, Solioz M (1999) Copper homeostasis in Enterococcus hirae. In: Copper Transport and Its Disorders. Springer USA. pp. 255–264Google Scholar
  161. Xue XM, Yan Y, Xu HJ, Wang N, Zhang X, Ye J (2014) ArsH from Synechocystis sp. PCC 6803 reduces chromate and ferric iron. FEMS Microbiol Lett 356:105–112PubMedCrossRefGoogle Scholar
  162. Yoon KP, Silver S (1991) A second gene in the Staphylococcus aureus cadA cadmium resistance determinant of plasmid pI258. J Bacteriol 173:7636–7642PubMedPubMedCentralGoogle Scholar
  163. Yu P, Yuan J, Deng X, Ma M, Zhang H (2014) Subcellular targeting of bacterial CusF enhances Cu accumulation and alters root to shoot Cu translocation in Arabidopsis. Plant Cell Physiol 55(9):1568–1581PubMedCrossRefGoogle Scholar
  164. Zhang YM, Yin H, Ye JS, Peng H, Zhang N, Qin HM, Yang F, He BY (2007) Cloning and expression of the nickel/cobalt transferase gene in E. coli BL21 and bioaccumulation of nickel ion by genetically engineered strain. Huan Jing Ke Xue 28(4):918–923PubMedGoogle Scholar
  165. Zhang W, Chen L, Liu D (2012) Characterization of a marine-isolated mercury resistant Pseudomonas putida strain SP1 and its potential application in marine mercury reduction. Appl Microbiol Biotechnol 93:1305–1314PubMedCrossRefGoogle Scholar
  166. Zhang H, Zhou Y, Bao H, Zhang L, Wang R, Zhou X (2015) Plasmid-borne cadmium resistant determinants are associated with the susceptibility of Listeria monocytogenes to bacteriophage. Microbiol Res 172:1–6PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Laboratory of Environmental Microbiology and Ecology (LEnME), Department of Life ScienceNational Institute of TechnologyRourkelaIndia

Personalised recommendations