Microbe-Mediated Removal of Heavy Metals for Sustainable Agricultural Practices

  • Ivy Mallick
  • Anupama Ghosh
  • Abhrajyoti GhoshEmail author
Part of the Soil Biology book series (SOILBIOL, volume 55)


Both environment and agriculture have been immensely affected by the sustaining humankind on Earth. Anthropogenic sources and natural calamities have increased toxic metal contents in the environment. This has also resulted in toxic metal accumulation within the food chain at an alarming concentration. The recalcitrant nature of these metals has threatened the living world. Thus, reclamation of the contaminated soils has become a global concern. Considering the cost involved and the production of hazardous by-products by the existing physiochemical techniques for cleanup of the polluted environment, newly emerged eco-friendly, cost-effective, and sustainable technologies are gaining attention. Use of indigenous microbes, bacteria prevalent in the rhizosphere, or plant-mediated removal of toxic metal is gaining attention as these processes are cost-effective and eco-friendly. Although there is an immense possibility to use bioremediation as a successful cleanup technology, it is yet to be extensively evaluated in the field conditions. Most of the studies aimed at the investigation of mechanistic details of bioremediation, relying mostly on the greenhouse-based laboratory results. Considering the hazard and complexity of toxic metal remediation, further studies on selecting suitable rhizosphere microbes along with exploring multidisciplinary approaches would provide new opportunities with promising success.



The authors duly acknowledge the support provided by an extramural grant [BT(Estt)/RD-3/2014] from the Department of Biotechnology, West Bengal, India, and a research grant of Ramanujan Fellowship to AG from the Science and Engineering Research Board (SERB), India (SR/S2/RJN-106/2012). IM was supported by Senior Research Assistantship from the Department of Biotechnology, West Bengal, India.


  1. Ahemad M (2012) Implications of bacterial resistance against heavy metals in bioremediation: a review. IIOAB J 3:39–46Google Scholar
  2. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20. CrossRefGoogle Scholar
  3. Ahmad I, Akhtar MJ, Asghar HN, Ghafoor U, Shahid M (2016) Differential effects of plant growth-promoting rhizobacteria on maize growth and cadmium uptake. J Plant Growth Regul 35(2):303–315. CrossRefGoogle Scholar
  4. Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91:869–881. CrossRefPubMedGoogle Scholar
  5. Alkorta I, Garbisu C (2001) Phytoremediation of organic contaminants in soils. Bioresour Technol 79:1994–1997CrossRefGoogle Scholar
  6. Arora K, Sharma S, Monti A (2016) Bio-remediation of Pb and Cd polluted soils by switchgrass: a case study in India. Int J Phytoremediation 18(7):704–709. CrossRefPubMedGoogle Scholar
  7. Azad MAK, Amin L, Sidik NM (2014) Genetically engineered organisms for bioremediation of pollutants in contaminated sites. Chin Sci Bull 59:703–714. CrossRefGoogle Scholar
  8. Azubuike CC, Chikere CB, Okpokwasili GC (2016) Bioremediation techniques-classification based on site of application: principles, advantages, limitations and prospects. World J Microbiol Biotechnol 32:180. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bae W, Mulchandani A, Chen W (2002) Cell surface display of synthetic phytochelatins using ice nucleation protein for enhanced heavy metal bioaccumulation. J Inorg Biochem 88:223–227CrossRefGoogle Scholar
  10. Bae W, Wu CH, Kostal J et al (2003) Enhanced mercury biosorption by bacterial cells with surface-displayed MerR. Appl Environ Microbiol 69:3176–3180CrossRefGoogle Scholar
  11. Banerjee S, Datta S, Chattyopadhyay D, Sarkar P (2011) Arsenic accumulating and transforming bacteria isolated from contaminated soil for potential use in bioremediation. J Environ Sci Health A Tox Hazard Subst Environ Eng 46:1736–1747. CrossRefPubMedGoogle Scholar
  12. Barkay T, Liebert C, Gillman M (1989) Environmental significance of the potential for mer(Tn21)-mediated reduction of Hg2+ to Hg0 in natural waters. Appl Environ Microbiol 55:1196–1202PubMedPubMedCentralGoogle Scholar
  13. Bentley R, Chasteen TG (2002) Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiol Mol Biol Rev 66:250–271CrossRefGoogle Scholar
  14. Beveridge TJ, Murray RG (1976) Uptake and retention of metals by cell walls of Bacillus subtilis. J Bacteriol 127:1502–1518PubMedPubMedCentralGoogle Scholar
  15. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350. CrossRefPubMedGoogle Scholar
  16. Bhattacharyya C, Bakshi U, Mallick I et al (2017) Genome-guided insights into the plant growth promotion capabilities of the physiologically versatile Bacillus aryabhattai strain AB211. Front Microbiol 8:1–16. CrossRefGoogle Scholar
  17. Birch L, Bachofen R (1990) Complexing agents from microorganisms. Experientia 46:827–834. CrossRefGoogle Scholar
  18. Brierley CL (1982) Microbiological mining. Sci Am 247:44–53CrossRefGoogle Scholar
  19. Brim H, McFarlan SC, Fredrickson JK et al (2000) Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments. Nat Biotechnol 18:85–90. CrossRefPubMedGoogle Scholar
  20. Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45:198–207. CrossRefPubMedGoogle Scholar
  21. Challenger F (1945) Biological methylation. Chem Rev 36:315–361. CrossRefGoogle Scholar
  22. Chang Y, Peacock AD, Long PE et al (2001) Diversity and characterization of sulfate-reducing bacteria in groundwater at a uranium mill tailings site. Appl Environ Microbiol 67:3149–3160. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Cifuentes FR, Lindemann WC, Barton LL (1996) Chromium sorption and reduction in soil with implications to bioremediation. Soil Sci 161:233–241CrossRefGoogle Scholar
  24. Dabrowska G, Hrynkiewicz K, Trejgell A, Baum C (2017) The effect of plant growth-promoting rhizobacteria on the phytoextraction of Cd and Zn by Brassica napus L. Int J Phytoremediation 19(7):597–604. CrossRefPubMedGoogle Scholar
  25. Das J, Sarkar P (2018) Remediation of arsenic in mung bean (Vigna radiata) with growth enhancement by unique arsenic-resistant bacterium Acinetobacter lwoffii. Sci Total Environ 624:1106–1118. CrossRefPubMedGoogle Scholar
  26. D’Souza SF (2001) Microbial biosensors. Biosens Bioelectron 16:337–353. CrossRefPubMedGoogle Scholar
  27. Dikshit A, Shukla SK, Mishra RK (2013) Exploring nanomaterials with PGPR in current agricultural scenario. Lambert Academic Publising, Saarbrucken, p 51Google Scholar
  28. Dombrowski PM, Long W, Farley KJ et al (2005) Thermodynamic analysis of arsenic methylation. Environ Sci Technol 39:2169–2176. CrossRefPubMedGoogle Scholar
  29. Fan Q, He J, Xue H et al (2007) Competitive adsorption, release and speciation of heavy metals in the Yellow River sediments, China. Environ Geol 53:239–251. CrossRefGoogle Scholar
  30. Fernández-Luqueño F, López-Valdez F, Gamero-Melo P et al (2013) Heavy metal pollution in drinking water – a global risk for human health: a review. Afr J Environ Sci Technol 7:567–584. CrossRefGoogle Scholar
  31. Flora SJ, Pachauri V (2010) Chelation in metal intoxication. Int J Environ Res Public Health 7:2745–2788. CrossRefPubMedPubMedCentralGoogle Scholar
  32. François F, Lombard C, Guigner JM et al (2012) Isolation and characterization of environmental bacteria capable of extracellular biosorption of mercury. Appl Environ Microbiol 78:1097–1106. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Fude L, Harris B, Urrutia MM, Beveridge TJ (1994) Reduction of Cr(VI) by a consortium of Sulfate-Reducing Bacteria (SRB III). Appl Environ Microbiol 60:1525–1531PubMedPubMedCentralGoogle Scholar
  34. Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643. CrossRefPubMedGoogle Scholar
  35. Gadd GM, White C (1993) Microbial treatment of metal pollution – a working biotechnology? Trends Biotechnol 11:353–359. CrossRefPubMedGoogle Scholar
  36. Garnham GW, Codd GA, Gadd GM (1992) Accumulation of cobalt, zinc and manganese by the estuarine green microalga Chlorella salina immobilized in alginate microbeads. Environ Sci Technol 26:1764–1770. CrossRefGoogle Scholar
  37. Glick BR, Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo) 2012:1–15. CrossRefGoogle Scholar
  38. Gontia-Mishra I, Sapre S, Sharma A, Tiwari S (2016) Alleviation of mercury toxicity in wheat by the interaction of mercury-tolerant plant growth-promoting rhizobacteria. J Plant Growth Regul 35(4):1000–1012. CrossRefGoogle Scholar
  39. Gouda S, Kerry RG, Das G et al (2018) Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol Res 206:131–140. CrossRefPubMedGoogle Scholar
  40. Gupta P, Diwan B (2017) Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnol Rep 13:58–71. CrossRefGoogle Scholar
  41. Gupta A, Joia J (2016) Microbes as potential tool for remediation of heavy metals: a review. J Microb Biochem Technol 8:364–372. CrossRefGoogle Scholar
  42. Hameed MSA (2006) Continuous removal and recovery of lead by alginate beads, free and alginate-immobilized Chlorella vulgaris. Afr J Biotechnol 5:1819–1823. CrossRefGoogle Scholar
  43. Han FX, Banin A, Su Y et al (2002) Industrial age anthropogenic inputs of heavy metals into the pedosphere. Naturwissenschaften 89:497–504. CrossRefPubMedGoogle Scholar
  44. Hansda A, Kumar V, Anshumali (2017) Cu-resistant Kocuria sp. CRB15: a potential PGPR isolated from the dry tailing of Rakha copper mine. 3 Biotech 7(2):132.
  45. Hassan TU, Bano A, Naz I (2017) Alleviation of heavy metals toxicity by the application of plant growth promoting rhizobacteria and effects on wheat grown in saline sodic field. Int J Phytoremediation 19(6):522–529. CrossRefPubMedGoogle Scholar
  46. He Z, Shentu YX et al (2015) Heavy metal contamination of soils: sources, indicators, and assessment. J Environ Indic 9:17–18Google Scholar
  47. Hemme CL, Green SJ, Rishishwar L, Prakash O, Pettenato A, Chakraborty R, Deutschbauer AM, Van Nostrand JD, Wu L, He Z, Jordan IK, Hazen TC, Arkin AP, Kostka JE, Zhou J (2016) Lateral gene transfer in a heavy metal-contaminated-groundwater microbial community. MBio 7:e02234-15. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Higham DP, Sadler PJ, Scawen MD (1984) Cadmium-resistant Pseudomonas putida synthesizes novel cadmium proteins. Science 225:1043–1046. CrossRefPubMedGoogle Scholar
  49. Higham DP, Sadler PJ, Scawen MD (1986) Cadmium-binding proteins in Pseudomonas putida: pseudothioneins. Environ Health Perspect 65:5–11PubMedPubMedCentralGoogle Scholar
  50. Hoyle B, Beveridge TJ (1983) Binding of metallic ions to the outer membrane of Escherichia coli. Appl Environ Microbiol 46:749–752PubMedPubMedCentralGoogle Scholar
  51. Hu B, Jia X, Hu J et al (2017) Assessment of heavy metal pollution and health risks in the soil-plant-human system in the Yangtze River Delta, China. Int J Environ Res Public Health 14:1042. CrossRefPubMedCentralGoogle Scholar
  52. Ianeva OD (2009) Mechanisms of bacteria resistance to heavy metals. Mikrobiol Z 71:54–65PubMedGoogle Scholar
  53. Ike A, Sriprang R, Ono H, Murooka Y, Yamashita M (2007) Bioremediation of cadmium contaminated soil using symbiosis between leguminous plant and recombinant rhizobia with the MTL4 and the PCS genes. Chemosphere 66(9):1670–1676. CrossRefPubMedGoogle Scholar
  54. Ike A, Sriprang R, Ono H, Murooka Y, Yamashita M (2008) Promotion of metal accumulation in nodule of Astragalus sinicus by the expression of the ironregulated transporter gene in Mesorhizobium huakuii subsp. rengei B3. J Biosci Bioeng 105(6):642–648. CrossRefPubMedGoogle Scholar
  55. Islam MS, Ueno Y, Sikder MT, Kurasaki M (2013) Phytofiltration of arsenic and cadmium from the water environment using Micranthemum Umbrosum (J.F. Gmel) S.F. Blake as a hyperaccumulator. Int J Phytoremediation 15:1010–1021. CrossRefPubMedGoogle Scholar
  56. Iyer A, Mody K, Jha B (2005) Biosorption of heavy metals by a marine bacterium. Mar Pollut Bull 50:340–343. CrossRefPubMedGoogle Scholar
  57. Jabeen R, Ahmad A, Iqbal M (2009) Phytoremediation of heavy metals: physiological and molecular mechanisms. Bot Rev 75:339–364. CrossRefGoogle Scholar
  58. Jan AT, Azam M, Ali A, Haq QMR (2014) Prospects for exploiting bacteria for bioremediation of metal pollution. Crit Rev Environ Sci Technol 44:519–560. CrossRefGoogle Scholar
  59. Jasrotia S, Kansal A, Mehra A (2017) Performance of aquatic plant species for phytoremediation of arsenic-contaminated water. Appl Water Sci 7:889. CrossRefGoogle Scholar
  60. Jelusic M, Lestan D (2015) Remediation and reclamation of soils heavily contaminated with toxic metals as a substrate for greening with ornamental plants and grasses. Chemosphere 138:1001–1007CrossRefGoogle Scholar
  61. Ji G, Silver S (1995) Bacterial resistance mechanisms for heavy metals of environmental concern. J Ind Microbiol 14:61–75CrossRefGoogle Scholar
  62. Jutsz AM, Gnida A (2015) Mechanisms of stress avoidance and tolerance by plants used in phytoremediation of heavy metals. Arch Environ Prot 41:104–114CrossRefGoogle Scholar
  63. Kawai H, Isobe Y, Horibe M et al (1992) Production of a novel extracellular polysaccharide by a Bacillus strain isolated from soil. Biosci Biotechnol Biochem 56:853–857. CrossRefPubMedGoogle Scholar
  64. Kazy SK, Sar P, Asthana RK, Singh SP (1999) Copper uptake and its compartmentalization in Pseudomonas aeruginosa strains: chemical nature of cellular metal. World J Microbiol Biotechnol 15:599–605. CrossRefGoogle Scholar
  65. Kim Y-J, Steenhuis TS, Nam K (2008) Movement of heavy metals in soil through preferential flow paths under different rainfall intensities. Clean (Weinh) 36:984–989. CrossRefGoogle Scholar
  66. Kolenbrander PE, Andersen RN, Baker RA, Jenkinson HF (1998) The adhesion-associated sca operon in Streptococcus gordonii encodes an inducible high-affinity ABC transporter for Mn2+ uptake. J Bacteriol 180:290–295PubMedPubMedCentralGoogle Scholar
  67. Komeda H, Kobayashi M, Shimizu S (1997) A novel transporter involved in cobalt uptake. Proc Natl Acad Sci USA 94:36–41CrossRefGoogle Scholar
  68. Kumar S, Dagar VK, Khasa YP, Kuhad RC (2013) Genetically Modified Microorganisms (GMOs) for bioremediation. In: Kuhad RC, Singh A (eds) Biotechnology for environmental management and resource recovery. Springer, New Delhi, pp 191–218CrossRefGoogle Scholar
  69. Limmer M, Burken J (2016) Phytovolatilization of organic contaminants. Environ Sci Technol 50(13):6632–6643. CrossRefPubMedGoogle Scholar
  70. Lloyd JR (2002) Bioremediation of metals: application of micro-organisms that make and break minerals. Microbiology 29:67–69Google Scholar
  71. Lloyd JR, Lovley DR (2001) Microbial detoxification of metals and radionuclides. Curr Opin Biotechnol 12:248–253CrossRefGoogle Scholar
  72. Lone MI, He Z, Stoffella PJ, Yang X (2008) Phytoremediation of heavy metal polluted soils and water: progresses and perspectives. J Zhejiang Univ Sci B 9:210–220. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Lovley DR, Coates JD (1997) Bioremediation of metal contamination. Curr Opin Biotechnol 8:285–289CrossRefGoogle Scholar
  74. Lozano LC, Dussán J (2013) Metal tolerance and larvicidal activity of Lysinibacillus sphaericus. World J Microbiol Biotechnol 29:1383–1389. CrossRefPubMedGoogle Scholar
  75. Macaskie LE (1991) The application of biotechnology to the treatment of wastes produced from the nuclear fuel cycle: biodegradation and bioaccumulation as a means of treating radionuclide-containing streams. Crit Rev Biotechnol 11:41–112. CrossRefPubMedGoogle Scholar
  76. Machado MD, Soares EV, Soares HMVM (2010) Removal of heavy metals using a brewer’s yeast strain of Saccharomyces cerevisiae: chemical speciation as a tool in the prediction and improving of treatment efficiency of real electroplating effluents. J Hazard Mater 180:347–353. CrossRefPubMedGoogle Scholar
  77. Mallick I, Mukherjee SK (2015) Bioremediation potential of an arsenic immobilizing strain Brevibacillus sp. KUMAs1 in the rhizosphere of chilli plant. Environ Earth Sci 74:6757–6765. CrossRefGoogle Scholar
  78. Mallick I, Hossain ST, Sinha S, Mukherjee SK (2014) Brevibacillus sp. KUMAs2, a bacterial isolate for possible bioremediation of arsenic in rhizosphere. Ecotoxicol Environ Saf 107:236–244. CrossRefPubMedGoogle Scholar
  79. Mallick I, Islam E, Kumar Mukherjee S (2015) Fundamentals and application potential of arsenic-resistant bacteria for bioremediation in rhizosphere: a review. Soil Sediment Contam 24:704–718. CrossRefGoogle Scholar
  80. Mallick I, Bhattacharyya C, Mukherji S, Dey D, Sarkar SC, Mukhopadhyay UK, Ghosh A (2018) Effective rhizoinoculation and biofilm formation by arsenic immobilizing halophilic plant growth promoting bacteria (PGPB) isolated from mangrove rhizosphere: A step towards arsenic rhizoremediation. Sci Total Environ 610–611:1239–1250. CrossRefPubMedGoogle Scholar
  81. McEntee JD, Woodrow JR, Quirk AV (1986) Investigation of cadmium resistance in an Alcaligenes sp. Appl Environ Microbiol 51:515–520PubMedPubMedCentralGoogle Scholar
  82. Mergeay M (1991) Towards an understanding of the genetics of bacterial metal resistance. Trends Biotechnol 9:17–24. CrossRefPubMedGoogle Scholar
  83. Merroun ML (2007) Interactions between metals and bacteria: fundamental and applied research. Commun Curr Res Educ Top Trends Appl Microbiol 4:108–119Google Scholar
  84. Michael GG (2008) Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. J Chem Technol Biotechnol 84:13–28. CrossRefGoogle Scholar
  85. Mishra AK, Roy P (2008) A note on the growth of Thiobacillus ferrooxidans on solid medium. J Appl Bacteriol 47:289–292. CrossRefGoogle Scholar
  86. Misra TK (1992) Bacterial resistances to inorganic mercury salts and organomercurials. Plasmid 27:4–16CrossRefGoogle Scholar
  87. Muszyńska E, Hanus-Fajerska E (2016) Why are heavy metal hyperaccumulating plants so amazing? Biotechnologia 96:265–271. CrossRefGoogle Scholar
  88. Nakajima A, Tsuruta T (2004) Competitive biosorption of thorium and uranium by Micrococcus luteus. J Radioanal Nucl Chem 260:13–18. CrossRefGoogle Scholar
  89. Navarro C, Wu LF, Mandrand-Berthelot MA (1993) The nik operon of Escherichia coli encodes a periplasmic binding-protein-dependent transport system for nickel. Mol Microbiol 9:1181–1191CrossRefGoogle Scholar
  90. Naz N, Young HK, Ahmed N, Gadd GM (2005) Cadmium accumulation and DNA homology with metal resistance genes in sulfate-reducing bacteria. Appl Environ Microbiol 71:4610–4618. CrossRefPubMedPubMedCentralGoogle Scholar
  91. Neilands JB (1981) Microbial iron compounds. Annu Rev Biochem 50:715–731. CrossRefPubMedGoogle Scholar
  92. Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750CrossRefGoogle Scholar
  93. Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14:186–199CrossRefGoogle Scholar
  94. Nies DH, Koch S, Wachi S et al (1998) CHR, a novel family of prokaryotic proton motive force-driven transporters probably containing chromate/sulfate antiporters. J Bacteriol 180:5799–5802PubMedPubMedCentralGoogle Scholar
  95. Novick RP (1967) Penicillinase plasmids of Staphylococcus aureus. Fed Proc 26:29–38PubMedGoogle Scholar
  96. O’Halloran TV (1993) Transition metals in control of gene expression. Science 261:715–725CrossRefGoogle Scholar
  97. Ojuederie OB, Babalola OO (2017) Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. Int J Environ Res Public Health 14:1504. CrossRefPubMedCentralGoogle Scholar
  98. Patzer SI, Hantke K (1998) The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28:1199–1210CrossRefGoogle Scholar
  99. Paulsen IT, Park JH, Choi PS, Saier MHJ (1997) A family of gram-negative bacterial outer membrane factors that function in the export of proteins, carbohydrates, drugs and heavy metals from gram-negative bacteria. FEMS Microbiol Lett 156:1–8CrossRefGoogle Scholar
  100. Placek A, Grobelak A, Kacprzak M (2016) Improving the phytoremediation of heavy metals contaminated soil by use of sewage sludge. Int J Phytoremediation 18:605–618CrossRefGoogle Scholar
  101. Pramanik K, Mitra S, Sarkar A, Soren T, Maiti TK (2017) Characterization of cadmium-resistant Klebsiella pneumoniae MCC 3091 promoted rice seedling growth by alleviating phytotoxicity of cadmium. Environ Sci Pollut Res Int 24(31):24419–24437. CrossRefPubMedGoogle Scholar
  102. Rahman MA, Hasegawa H (2011) Aquatic arsenic: phytoremediation using floating macrophytes. Chemosphere 83(5):633–646CrossRefGoogle Scholar
  103. Rajapaksha AU, Vithanage M, Ok YS, Oze C (2013) Cr(VI) formation related to Cr(III)-muscovite and birnessite interactions in ultramafic environments. Environ Sci Technol 47:9722–9729. CrossRefPubMedGoogle Scholar
  104. Ramasamy K, Parwin Banu S (2007) Bioremediation of metals: microbial processes and techniques. In: Environmental bioremediation technologies. Springer, Berlin. CrossRefGoogle Scholar
  105. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181. CrossRefPubMedGoogle Scholar
  106. Rensing C, Mitra B, Rosen BP (1997) The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc Natl Acad Sci USA 94:14326–14331CrossRefGoogle Scholar
  107. Román-Ponce B, Reza-Vázquez DM, Gutiérrez-Paredes S, De Jesús De Haro-Cruz M, Maldonado-Hernández J, Bahena-Osorio Y, Estrada-De Los Santos P, Wang ET, Vásquez-Murrieta MS (2017) Plant growth-promoting traits in rhizobacteria of heavy metal-resistant plants and their effects on Brassica nigra seed germination. Pedosphere 27(3):511–526. CrossRefGoogle Scholar
  108. Rouch DA, Lee BT, Morby AP (1995) Understanding cellular responses to toxic agents: a model for mechanism-choice in bacterial metal resistance. J Ind Microbiol 14:132–141CrossRefGoogle Scholar
  109. Saier MHJ (1994) Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, and evolution. Microbiol Rev 58:71–93PubMedPubMedCentralGoogle Scholar
  110. Saier MHJ, Tam R, Reizer A, Reizer J (1994) Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol Microbiol 11:841–847CrossRefGoogle Scholar
  111. Salido AL, Hasty KL, Lim J-M, Butcher DJ (2003) Phytoremediation of arsenic and lead in contaminated soil using Chinese brake ferns (Pteris vittata) and Indian mustard (Brassica juncea). Int J Phytoremediation 5(2):89–103. CrossRefPubMedGoogle Scholar
  112. Sar P, Kazy SK, Singh SP (2001) Intracellular nickel accumulation by Pseudomonas aeruginosa and its chemical nature. Lett Appl Microbiol 32:257–261CrossRefGoogle Scholar
  113. Sato T, Kobayashi Y (1998) The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J Bacteriol 180:1655–1661PubMedPubMedCentralGoogle Scholar
  114. Scott JA, Palmer SJ (1990) Sites of cadmium uptake in bacteria used for biosorption. Appl Microbiol Biotechnol 33:221–225CrossRefGoogle Scholar
  115. Sheila RM (1994) Toxic metals in soil-plant systems. Wiley, ChichesterGoogle Scholar
  116. Silver S, Ji G (1994) Newer systems for bacterial resistances to toxic heavy metals. Environ Health Perspect 102(Suppl):107–113PubMedPubMedCentralGoogle Scholar
  117. Silver S, Misra TK (1984) Bacterial transformations of and resistances to heavy metals. Basic Life Sci 28:23–46PubMedGoogle Scholar
  118. Silver S, Phung LT (1996) Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol 50:753–789. CrossRefPubMedGoogle Scholar
  119. Silver S, Walderhaug M (1992) Gene regulation of plasmid- and chromosome-determined inorganic ion transport in bacteria. Microbiol Rev 56:195–228PubMedPubMedCentralGoogle Scholar
  120. Singh SK, Grass G, Rensing C, Montfort WR (2004) Cuprous oxidase activity of CueO from Escherichia coli cuprous oxidase activity of CueO from Escherichia coli. J Bacteriol 186:7815–7817. CrossRefPubMedPubMedCentralGoogle Scholar
  121. Sinha S, Mukherjee SK (2009) Pseudomonas aeruginosa KUCD1, a possible candidate for cadmium bioremediation. Braz J Microbiol 40:655–662. CrossRefPubMedPubMedCentralGoogle Scholar
  122. Sinha RK, Valani D, Sinha S, Singh S, Herat S (2009) Bioremediation of contaminated sites: a low-cost nature’s biotechnology for environmental clean up by versatile microbes, plants & earthworms. In: Faerber T, Herzog J (eds) Solid waste manage-ment and environmental remediation. Nova Science Publishers Inc, New York. ISBN: 978-1-60741-761-3Google Scholar
  123. Smith RL, Maguire ME (1995) Distribution of the CorA Mg2+ transport system in gram-negative bacteria. J Bacteriol 177:1638–1640CrossRefGoogle Scholar
  124. Smith RL, Gottlieb E, Kucharski LM, Maguire ME (1998) Functional similarity between archaeal and bacterial CorA magnesium transporters. J Bacteriol 180:2788–2791PubMedPubMedCentralGoogle Scholar
  125. Smith AH, Lingas EO, Rahman M (2000) Contamination of drinking-water by arsenic in Bangladesh: a public health emergency. Bull World Health Organ 78:1093–1103PubMedPubMedCentralGoogle Scholar
  126. Snavely MD, Florer JB, Miller CG, Maguire ME (1989) Magnesium transport in Salmonella typhimurium: 28Mg2+ transport by the CorA, MgtA, and MgtB systems. J Bacteriol 171:4761–4766CrossRefGoogle Scholar
  127. Spain A, Alm E (2003) Implications of microbial heavy metal tolerance in the environment. Rev Undergrad Res 2:1–6Google Scholar
  128. Spark KM, Wells JD, Johnson BB (1997) The interaction of a humic acid with heavy metals. Soil Res 35:89–102CrossRefGoogle Scholar
  129. Sriprang R, Hayashi M, Ono H, Takagi M, Hirata K, Murooka Y (2003) Enhanced accumulation of Cd(2+) by a Mesorhizobium sp. transformed with a gene from arabidopsis thaliana coding for phytochelatin synthase. Appl Environ Microbiol 69(3):1791–1796. CrossRefPubMedPubMedCentralGoogle Scholar
  130. Stan V, Gament E, Cornea CP et al (2011) Effects of heavy metal from polluted soils on the Rhizobium diversity. Not Bot Horti Agrobot Cluj-Napoca 39:88–95. CrossRefGoogle Scholar
  131. Su C, Jiang L, Zhang W (2014) A review on heavy metal contamination in the soil worldwide: situation, impact and remediation techniques. Environ Skept Critics 3:24–38. CrossRefGoogle Scholar
  132. Subramanian KS, Tarafdar JC (2011) Prospects of nanotechnology in Indian farming. Indian J Agric Sci 81:887–893Google Scholar
  133. Summers AO, Silver S (1978) Microbial transformations of metals. Annu Rev Microbiol 32:637–672. CrossRefPubMedGoogle Scholar
  134. Sylvain B, Motelica-Heino M, Florie M, Joussein E, Soubrand-Colin M, Sylvain B et al (2016) Phytostabilization of As, Sb and Pb by two willow species (S. viminalis and S. purpurea) on former mine technosols. Catena 136:44–52. CrossRefGoogle Scholar
  135. Tandon PK, Singh SB (2016) Redox processes in water remediation. Environ Chem Lett 14:15–25. CrossRefGoogle Scholar
  136. Tebo BM, Ghiorse WC, van Waasbergen LG et al (1997) Bacterially mediated mineral formation; insights into manganese(II) oxidation from molecular genetic and biochemical studies. Rev Mineral Geochem 35:225–266Google Scholar
  137. Thayer JS (2004) Methylation: its role in the environmental mobility of heavy elements. Appl Organomet Chem 3:123–128. CrossRefGoogle Scholar
  138. Trevors JT, Oddie KM, Belliveau BH (1985) Metal resistance in bacteria. FEMS Microbiol Rev 1:39–54CrossRefGoogle Scholar
  139. Turpeinen R (2002) Interactions between metals, microbes andplants: bioremediation of arsenic and lead contaminated soils, MSc Dissertation in Environmental Ecology, Fac. Sci., Univ. HelsinkiGoogle Scholar
  140. Vassilev A, Schwitzguebel JP, Thewys T et al (2004) The use of plants for remediation of metal-contaminated soils. ScientificWorldJournal 4:9–34. CrossRefPubMedPubMedCentralGoogle Scholar
  141. Verma N, Singh M (2005) Biosensors for heavy metals. Biometals 18:121–129. CrossRefPubMedGoogle Scholar
  142. Vithanage M, Dabrowska BB, Mukherjee AB, Sandhi A, Bhattacharya P (2012) Arsenic uptake by plants and possible phytoremediation applications: a brief overview. Environ Chem Lett 10:217–224CrossRefGoogle Scholar
  143. Volesky B, Holan ZR (1995) Biosorption of heavy metals. Biotechnol Prog 11:235–250. CrossRefPubMedGoogle Scholar
  144. Wakatsuki T (1995) Metal oxidoreduction by microbial cells. J Ind Microbiol 14:169–177CrossRefGoogle Scholar
  145. Wang J, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotechnol Adv 27:195–226. CrossRefPubMedGoogle Scholar
  146. Weiss AA, Silver S, Kinscherf TG (1978) Cation transport alteration associated with plasmid-determined resistance to cadmium in Staphylococcus aureus. Antimicrob Agents Chemother 14:856–865CrossRefGoogle Scholar
  147. White C, Gadd GM (1990) Biosorption of radionuclides by fungal biomass. J Chem Technol Biotechnol 49:331–343CrossRefGoogle Scholar
  148. White C, Sayer JA, Gadd GM (1997) Microbial solubilization and immobilization of toxic metals: key biogeochemical processes for treatment of contamination. FEMS Microbiol Rev 20:503–516CrossRefGoogle Scholar
  149. White C, Sharman AK, Gadd GM (1998) An integrated microbial process for the bioremediation of soil contaminated with toxic metals. Nat Biotechnol 16:572–575. CrossRefPubMedGoogle Scholar
  150. Wolfram L, Friedrich B, Eitinger T (1995) The Alcaligenes eutrophus protein HoxN mediates nickel transport in Escherichia coli. J Bacteriol 177:1840–1843CrossRefGoogle Scholar
  151. Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol 2011:1–20. CrossRefGoogle Scholar
  152. Wu CH, Wood TK, Mulchandani A, Chen W (2006) Engineering plant-microbe symbiosis for rhizoremediation of heavy metals. Appl Environ Microbiol 72(2):1129–1134. CrossRefPubMedPubMedCentralGoogle Scholar
  153. Yong X, Chen Y, Liu W, Xu L, Zhou J, Wang S, Chen P, Ouyang P, Zheng T (2014) Enhanced cadmium resistance and accumulation in Pseudomonas putida KT2440 expressing the phytochelatin synthase gene of Schizosaccharomyces pombe. Lett Appl Microbiol 58(3):255–261. CrossRefPubMedGoogle Scholar
  154. Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413. CrossRefPubMedGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of BiochemistryBose InstituteKolkataIndia
  2. 2.Division of Plant BiologyBose InstituteKolkataIndia

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