Rhizobacteria: Restoration of Heavy Metal-Contaminated Soils

  • Seifeddine Ben Tekaya
  • Sherlyn Tipayno
  • Kiyoon Kim
  • Parthiban Subramanian
  • Tongmin Sa
Chapter
First Online:

Abstract

Heavy metal pollution has become one of the major culprits of environmental disasters. Their toxicity and damaging effects on soils and agricultural lands and direct impact on human health through soils and agricultural lands are considered a major world challenge. Many removal processes, such as mechanical and physicochemical ones have been introduced. However, because of their high cost, attention has been focused on biological solutions, which are less expensive and more efficient. Interestingly, some microorganisms have shown high potential to metal tolerance and removal. Cupriavidus metallidurans is certainly the most known example. The rhizosphere, an important interface between soil and plant, holds a diverse prokaryotic microflora population known as rhizobacteria. An important fraction of these microorganisms have been found to be involved in the removal of heavy metals through a panoply of mechanisms including release of chelating substances, microenvironment acidification, and promotion of redox potentials. The different mechanisms of resistance and interactions with metals have also been discussed. It has been also shown that rhizospheric bacteria may play beneficial roles in phytoremediation processes via facilitating bioavailability of heavy metals to plants such as maize and tomato, as well as for metal stress alleviation along rhizosphere of sensitive crops. In this chapter, we focused on the potentials of rhizobacteria for restoration of metal-affected soils and their role in improving metal uptake for phytoremediation processes. Because of the advantages of being less costly and environmental friendly, microbes are still the best tool for metal removal. But as living organisms, subject to death and decomposition through the geochemical cycles in the soil, their metal cleaning processes are never perfect and the removal may be tentative or not definitive. One of the foci now is on microbial bioengineering and genetic improvement of rhizobacteria and other soil microbial abilities for metal handling. Among the various microbial phyla in the rhizosphere, actinobacteria have drawn great interest due to their high biological compound production, which confer adaptation to a wide spectrum of ecological conditions, including metal contamination in soils. Their extremophilic traits and biological competitiveness in soil present them as possible efficient candidate for bioremediation. We included here their plant growth promotion capacity as well as their potentials for metal bioremediation.

Keywords

Heavy Metal Metal Uptake Metal Removal Plant Growth Promotion Metal Stress 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

The authors would like to thank Dr. Murugesan Chandrasekaran for critical review and helpful comments. We are also thankful to the reviewer for useful comments on the previous version of this book chapter.

References

  1. Abou-Shanab RA, Ghozlan H, Ghanem K, Moawad H (2005) Behaviour of bacterial populations isolated from rhizosphere of Diplachne fusca dominant in industrial sites. World J Microbiol Biotechnol 21:1095–1101Google Scholar
  2. Aldesuquy HS, Mansour FA, Abo-Hamed SA (1998) Effect of the culture filtrates of Streptomyces on growth and productivity of wheat plants. Folia Microbiol 43:465–470Google Scholar
  3. Alkorta I, Garbisu C (2001) Phytoremediation of organic contaminants in soils. Bioresour Technol 79:273–276PubMedGoogle Scholar
  4. Arshad M, Saleem M, Hussain S (2007) Perspectives of bacterial ACC deaminase in phytoremediation. Trends Biotechnol 25:356–362PubMedGoogle Scholar
  5. Avery S (1995) Microbial interactions with caesium—implications for biotechnology. J Chem Technol Biotechnol 62:3–16Google Scholar
  6. Barkay T, Schaefer J (2001) Metal and radionuclide bioremediation: issues, considerations and potential. Curr Opin Microbiol 4:318–323PubMedGoogle Scholar
  7. Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384PubMedGoogle Scholar
  8. Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ (2008) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signaling. New Phytol 181:413–423Google Scholar
  9. Beolchini F, Fonti V, Rocchetti L, Saraceni G, Pietrangeli B, Dell’Anno A (2013) Chemical and biological strategies for the mobilisation of metals/semi-metals in contaminated dredged sediments: experimental analysis and environmental impact assessment. Chem Ecol 29(5):415–426Google Scholar
  10. Borges-Walmsley MI, Mckeegan KS, Walmsley AR (2003) Structure and function of efflux pumps that confer resistance to drugs. Biochem J 376:313–338PubMedGoogle Scholar
  11. Braud A, Jezequel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286PubMedGoogle Scholar
  12. Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45:198–207PubMedGoogle Scholar
  13. Canovas D, Cases I, Lorenzo V (2003) Heavy metal tolerance and metal homeostasis in Pseudomonas putida as revealed by complete genome analysis. Environ Microbiol 5:1242–1256PubMedGoogle Scholar
  14. Cindy HW, Wood TK, Mulchandani A, Chen W (2006) Engineering plant-microbe symbiosis for rhizoremediation of heavy metals. Appl Environ Microbiol 72:1129–1134Google Scholar
  15. Colin LV, Liliana BV, Abate CM (2012) Indigenous microorganisms as potential bioremediators for environments contaminated with heavy metals. Int Biodeterior Biodegrad 69:28–37Google Scholar
  16. Colin LV, Pereira CE, Villegas LB, Amoroso MJ, Abate CM (2013) Production and partial characterization of bioemulsifier from a chromium-resistant actinobacteria. Chemosphere 90:1372–1378PubMedGoogle Scholar
  17. Compant S, Clement C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678Google Scholar
  18. Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071PubMedGoogle Scholar
  19. Copping LG, Duke SO (2007) Natural products that have been used commercially as crop protection agents. Pest Manag Sci 63:524–554PubMedGoogle Scholar
  20. Cunningham SD, Berti WR, Huang JW (1995) Phytoremediation of contaminated soils. Trends Biotechnol 13:393–397Google Scholar
  21. Dash HR, Das S (2012) Bioremediation of mercury and importance of bacterial mer genes. Int Biodeterior Biodegrad 75:207–213Google Scholar
  22. De Carvalho Costa FE, Soares De Melo I (2012) Endophytic and rhizospheric bacteria from Opuntia ficus-indica mill and their ability to promote plant growth in cowpea, Vigna unguiculata (L.) walp. Afr J Microbiol Res 6:1345–1353Google Scholar
  23. Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40:74–84Google Scholar
  24. Delvasto P, Ballester A, Munoz JA, Gonzalez F, Blazquez ML, Igual JM, Valverde A (2009) Mobilization of phosphorus from iron ore by the bacterium Burkholderia caribensis FeGL03. Miner Eng 22:1–9Google Scholar
  25. Dimkpa CO, Merten D, Svatos A, Buchel G, Kothe E (2009) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162Google Scholar
  26. Doumbou CL, Hamby Salove MK, Crawford DL, Beaulieu C (2011) Actinomycetes, promising tools to control plant diseases and to promote plant growth. Phytoprotection 82:85–102Google Scholar
  27. Duffus JH (2002) Heavy metals: a meaningless term? Pure Appl Chem 74:793–807Google Scholar
  28. Egamberdieva D (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant 31:861–864Google Scholar
  29. Ehrlich HL (1997) Microbes and metals. Appl Microbiol Biotechnol 48:687–692Google Scholar
  30. El-Tarabily KA, Krishnapillai S (2006) Non-Streptomyces actinomycetes as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Soil Biol Biochem 38:1505–1520Google Scholar
  31. El-Tarabily KA, Hardy GEST, Sivasithamparam K, Hussein AM, Kurtboke DI (1997) The potential for the biological control of cavity-spot disease of carrots, caused by Pythium cloratum, by Streptomyces and non-Streptomyces actinomycetes. New Phytol 137:495–507Google Scholar
  32. El-Tarabily KA, Soliman MH, Nassar AH, Al-Hassani HA, Sivasithamparam K, McKenna F, Hardy GEST (2000) Biological control of Sclerotinia minor using a chitinolytic bacterium and actinomycetes. Plant Pathol 49:573–583Google Scholar
  33. El-Tarabily KA, Hardy GEST, Sivasithamparam K (2010) Performance of three endophytic actinomycetes in relation to plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber under commercial field production conditions in the United Arab Emirates. Eur J Plant Pathol 128:527–539Google Scholar
  34. Faisal M, Hasnain S (2006) Growth stimulatory effect of Ochrobactrum intermedium and Bacillus cereus on Vigna radiata plants. Lett Appl Microbiol 43:461–466PubMedGoogle Scholar
  35. Finneran KT, Housewright ME, Lovley DR (2002) Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environ Microbiol 4:510–516PubMedGoogle Scholar
  36. Fogarti RV, Tobin JM (1996) Fungal melanins and their interactions with metals. Enzyme Microb Technol 19:311–317Google Scholar
  37. Francis I, Holsters M, Vereecke D (2010) The gram positive side of plant-microbe interactions. Environ Microbiol 12:1–12PubMedGoogle Scholar
  38. Gadd GM (2004) Microbial influence on metal mobility and application for bioremediation. Geoderma 122:109–119Google Scholar
  39. Gadd GM (2008) Transformation and mobilization of metals, metalloids, and radionuclides by microorganisms. In: Violante A, Huang PM, Gadd GM (eds) Biophysico-chemical processes of heavy metals and metalloids in soil environments. Wiley, New York, pp 53–96Google Scholar
  40. Ghodhbane-Gtari F, Essoussi I, Chattaoui M, Chouaia B, Jaouani A, Daffonchio D, Boudabous A, Gtari M (2010) Isolation and characterization of non-Frankia actinobacteria from root nodules of Alnus glutinosa, Casuarina glauca and Elaeagnus angustifolia. Symbiosis 50:51–57Google Scholar
  41. Ghosh S, Penterman JM, Little RD, Chavez R, Glick BR (2003) Three newly isolated plant growth-promoting bacilli facilitate the seedling growth of canola, Brassica campestris. Plant Physiol Biochem 41:277–281Google Scholar
  42. Giller KE, Witter E, Mcgrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414Google Scholar
  43. Glick BR (2003) Phytoremediation: synergetic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393PubMedGoogle Scholar
  44. Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374PubMedGoogle Scholar
  45. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68PubMedGoogle Scholar
  46. Goodnight CJ (2000) Heritability of the ecosystem level. Proc Natl Acad Sci U S A 97:9365–9366PubMedGoogle Scholar
  47. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol Biochem 37:395–412Google Scholar
  48. Gremion F, Chatzinotas A, Harms H (2003) Comparative 16s rDNA and rRNA sequence analysis indicates that actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal-contaminated bulk and rhizosphere soil. Environ Microbiol 5:896–907PubMedGoogle Scholar
  49. Gtari M, Essoussi I, Maaoui R, Sghaier H, Boujmil R, Gury J, Pujic P, Brusetti L, Chouaia B, Crotti E, Daffonchio D, Boudabous A, Normand P (2012) Contrasted resistance of stone-dwelling Geodermatophilaceae species to stresses known to give rise to reactive oxygen species. FEMS Microbiol Ecol 80:566–577PubMedGoogle Scholar
  50. Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47:453–467PubMedGoogle Scholar
  51. Hamaki T, Suzuki R, Fudou Y, Jojima T, Kajiura A, Tabuchi KS, Shibai H (2005) Isolation of novel bacteria and actinomycetes using soil-extract agar medium. J Biosci Bioeng 99:485–492PubMedGoogle Scholar
  52. Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008) Rock phosphate-solubilizing actinomycetes: screening for plant growth-promoting activities. World J Microbiol Biotechnol 24:2565–2575Google Scholar
  53. Hardoim PR, Overbeek LSV, Van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471PubMedGoogle Scholar
  54. Horitsu H, Takagi M, Tomoyeda M (1978) Isolation of a mercuric chloride-tolerant bacterium and uptake of mercury by the bacterium. Eur J Appl Microbiol 5:279–290Google Scholar
  55. Huang Q, Jianmei W, Wenli C, Xueyuan L (2000) Adsorption of cadmium by soil colloids and minerals in presence of rhizobia. Pedosphere 10:299–307Google Scholar
  56. Jarup L (2003) Hazards of heavy metals contamination. Br Med Bull 68:167–182PubMedGoogle Scholar
  57. Joshi PM, Juwarkar AA (2009) In vivo studies to elucidate the role of extracellular polymeric substances from Azotobacter in immobilization of heavy metals. Environ Sci Technol 43:5884–5889PubMedGoogle Scholar
  58. Kalinowski BE, Oskarsson A, Albinsson Y, Arlinger J, Odegaard-Jensen A, Andlid T, Pedersen K (2004) Microbial leaching of uranium and other trace elements from shale mine tailings at Ranstad. Geoderma 122:177–194Google Scholar
  59. Karelova E, Harichova J, Stojnev T, Pangallo D, Ferianc P (2011) The isolation of heavy-metal resistant culturable bacteria and resistance determinants from a heavy-metal contaminated site. Biologia 1:18–26Google Scholar
  60. Khamna S, Yokota A, Lumyong S (2009) Actinomycetes isolated from medicinal plant rhizosphere soils: diversity and screening of antifungal compounds, indole-3-acetic acid and siderophore production. World J Microbiol Biotechnol 25:649–655Google Scholar
  61. Khan AG (2005) Role of soil microbes in the rhizosphere of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364PubMedGoogle Scholar
  62. Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19Google Scholar
  63. Khan MS, Zaidi A, Wani PA, Oves M (2010) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils: a review. In: Lichtfous E (ed) Organic farming, pest control and remediation of soil pollutants sustainable agriculture reviews. Springer, The Netherlands, pp 319–350Google Scholar
  64. Kong S, Johnstone DL, Yonge DR, Petersen JN, Brouns TM (1994) Long-term intracellular chromium partitioning with subsurface bacteria. Appl Microbiol Biotechnol 42:403–407Google Scholar
  65. Kumar A (2012) Role of plant-growth-promoting rhizobacteria in the management of cadmium-contaminated soil. In: Zaidi A et al (eds) Toxicity of heavy metals to legumes and bioremediation. Springer, Wien, pp 163–178Google Scholar
  66. Kumar KV, Patra DD (2013) Effect of metal tolerant plant growth promoting bacteria on growth and metal accumulation in Zea mays plants grown in fly ash amended soil. Int J Phytoremediation 15:743–755PubMedGoogle Scholar
  67. Lakzian A, Murphy P, Turner A, Beynon JL, Giller KE (2002) Rhizobium leguminozarum bv. Viciae populations in soils increasing heavy metal contamination: abundance, plasmid profiles, diversity and metal tolerance. Soil Biol Biochem 34:519–529Google Scholar
  68. Lambrecht M, Okon Y, Vande Broek A, Vanderleyden J (2000) Indole-3 acetic acid: a reciprocal signalling molecule in bacteria-plant interactions. Trends Microbiol 8:298–300PubMedGoogle Scholar
  69. Langley S, Beveridge TJ (1999) Metal binding by Pseudomonas aeruginosa PAO1 is influenced by growth of the cells as a biofilm. Can J Microbiol 45:616–622PubMedGoogle Scholar
  70. Larkin M, Kulakov LA, Allen CCR (2005) Biodegradation and Rhodococcus—masters of catabolic versatility. Curr Opin Biotechnol 16:282–290PubMedGoogle Scholar
  71. Lazzaro A, Widmer F, Sperisen C, Frey B (2008) Identification of dominant bacterial phylotypes in a cadmium-treated forest soil. FEMS Microbiol Ecol 63:143–155PubMedGoogle Scholar
  72. Ledin M (2000) Accumulation of metals by microorganisms—processes and importance for soil systems. Earth Sci Rev 51:1–31Google Scholar
  73. Lee J, Postmaster A, Peng Soon H, Keast D, Carson KC (2012) Siderophore production by actinomycetes isolated from two soil sites in western Australia. Biometals 25:285–296PubMedGoogle Scholar
  74. Li PF, Qiu GL, Shang LH, Li ZG (2009) Mercury pollution in Asia: a review of the contaminated sites. J Hazard Mater 168:591–601PubMedGoogle Scholar
  75. Lippmann B, Leinhos V, Bergmann H (1995) Influence of auxin producing rhizobacteria on root morphology and nutrient accumulation of crops, pt. 1: changes in root morphology and nutrient accumulation in maize (Zea mays L.) caused by inoculation with indole-3 acetic acid (IAA) producing Pseudomonas and Acinetobacter strains or IAA applied exogenously. Angew Bot 69:31–36Google Scholar
  76. Lovley DR, Lloyd JR (2000) Microbes with a mettle for bioremediation. Nat Biotechnol 18:600–601PubMedGoogle Scholar
  77. Ma Y, Rajkumar M, Freitas H (2009) Inoculation of plant growth promotion bacterium Achromobacter xylosoxidans strain Ax10 for the improvement of copper phytoextraction by Brassica juncea. J Environ Manage 90:831–837PubMedGoogle Scholar
  78. Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258PubMedGoogle Scholar
  79. Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69:220–228PubMedGoogle Scholar
  80. Madhaiyan M, Poonguzhali S, Lee JS, Senthilkumar M, Lee KC, Sundaram S (2010) Leifsonia soli sp. nov., a yellow-pigmented actinobacterium isolated from teak rhizosphere soil. Int J Syst Evol Microbiol 60:1322–1327PubMedGoogle Scholar
  81. Maier RJ, Pihl TD, Stults L, Sray W (1990) Nickel accumulation and storage in Bradyrhizobium japonicum. Appl Environ Microbiol 56:1905–1911PubMedGoogle Scholar
  82. Marta AP, Amoroso MJ, Abate CM (2011) Intracellular chromium accumulation by Streptomyces sp. MC1. Water Air Soil Pollut 214:49–57Google Scholar
  83. Martins SJ, De Medeiros FHV, De Souza RM, De Resende MLV, Junior PMR (2013) Biological control of bacterial wilt of common bean by plant growth-promoting rhizobacteria. Biol Control 66(1):65–71Google Scholar
  84. Mastretta C, Taghavi S, Van Der Lelie D, Mengoni A, Galardi F, Gonnelli C, Barac T, Boulet J, Nele W, Vangronsveld J (2009) Endophytic bacteria from seeds of Nicotina tabacum can reduce cadmium phytotoxicity. Int J Phytoremediation 11:251–267Google Scholar
  85. Minami R, Uchiyama K, Murakami T, Kawai J, Mikami K, Yamada T, Yokoi D, Ito H, Matsui H, Honma M (1998) Properties, sequence, and synthesis in Escherichia coli of 1-aminocyclopropane-1-carboxylate deaminase from Hansenula saturnus. J Biochem 123:1112–1118PubMedGoogle Scholar
  86. Naees M, Ali Q, Shahbaz M, Ali F (2011) Role of rhizobacteria in phytoremediation of heavy metals: an overview. Int Res J Plant Sci 2:220–232Google Scholar
  87. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726PubMedGoogle Scholar
  88. Nele W, Van Der Lelie D, Safiyh T, Jaco V (2009) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254Google Scholar
  89. Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750PubMedGoogle Scholar
  90. Nies DH (2006) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339Google Scholar
  91. Nimnoi P, Pongsilp N, Lumyong S (2010) Endophytic actinomycetes isolated from Aquilaria crassna Pierre ex Lec and screening of plant growth promoters production. World J Microbiol Biotechnol 26:193–203Google Scholar
  92. Nosanchuk JD, Casadevall A (2003) The contribution of melanin to microbial pathogenesis. Cell Microbiol 5:203–223PubMedGoogle Scholar
  93. Okino S, Iwasaki K, Yagi O, Tanaka H (2000) Development of a biological mercury removal-recovery system. Biotechnol Lett 22:783–788Google Scholar
  94. Palanché T, Blanc S, Hennard C, Abdallah MA, Albrecht-Gary AM (2004) Bacterial iron transport: coordination properties of azotobactin, the highly fluorescent siderophore of Azotobacter vinelandii. Inorg Chem 43:1137–1152PubMedGoogle Scholar
  95. Panday B, Ghimire P, Prasad Agrawal V (2004) Studies on the antibacterial activities of the actinomycetes isolated from the khumbu region of Nepal. J Biol Sci 23:44–53Google Scholar
  96. Patel HA, Patel RK, Khristi SM, Parikh K, Rajendran G (2012) Isolation and characterization of bacterial endophytes from Lycopersicon esculentum plant and their plant growth promoting characteristics. Nepal J Biotechnol 2:37–52Google Scholar
  97. Paul AK, Banerjee AK (1983) Determination of optimum conditions for antibiotic production by Streptomyces galbus. Folia Microbiol 28:397–405Google Scholar
  98. Purakayastha TJ (2011) Microbial remediation of arsenic contaminated soils. In: Sherameti I, Varma A (eds) Detoxification of heavy metals, soil biology, vol 30. Springer, Berlin, pp 221–260Google Scholar
  99. Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574PubMedGoogle Scholar
  100. Reichman SM (2007) The potential use of the legume-rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol Biochem 39:2587–2593Google Scholar
  101. Rensing C, Sun Y, Mitra B, Rosen BP (1998) Pb(II)-translocating P-type ATPases. J Biol Chem 273:32614–32617PubMedGoogle Scholar
  102. Richards JW, Krumholz GD, Chval MS, Tisa LS (2002) Heavy metal resistance patterns of Frankia strains. Appl Environ Microbiol 68:923–927PubMedGoogle Scholar
  103. Riley PA (1997) Molecules in focus melanin. Int J Biochem Cell Biol 29:1235–1239PubMedGoogle Scholar
  104. Robinson B, Russells C, Hedley M, Clothier B (2001) Cadmium adsorption by rhizobacteria: implications for New Zealand pastureland. Agr Ecosyst Environ 87:315–321Google Scholar
  105. Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92PubMedGoogle Scholar
  106. Rosen BP, Ambudkar SV, Borbolla MG, Chen CM, Houng HS, Mobley HLT, Tsujibo H, Zlontnick GW (1985) Ion extrusion system in bacteria. Ann N Y Acad Sci 456:235–244PubMedGoogle Scholar
  107. Rouch DA, Lee BTO, Morby AP (1995) Understanding cellular responses to toxic agents: a model for mechanism-choice in bacterial metal resistance. J Ind Microbiol 14:132–141PubMedGoogle Scholar
  108. Ruanpanum P, Tangchitsomkid N, Hyde KD, Lumyong S (2010) Actinomycetes and fungi isolated from plant-parasitic nematode infested soils: screening of the effective biocontrol potential, indole-3-acetic acid and siderophore production. World J Microbiol Biotechnol 26:1569–1578Google Scholar
  109. Ruiz-Diez B, Quinones MA, Fajardo S, Lopez MA, Higueras P, Fernandez-Pacual M (2012) Mercury-resistant rhizobial bacteria isolated from nodules of leguminous plants growing in high Hg-contaminated soils. Appl Microbiol Biotechnol 96:543–554PubMedGoogle Scholar
  110. Samuelson P, Wernerus H, Svedberg M, Stahl S (2000) Staphylococcal surface display of metal-binding polyhistidyl peptides. Appl Environ Microbiol 66:1243–1248PubMedGoogle Scholar
  111. Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, Del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126PubMedGoogle Scholar
  112. Saravanan VS, Madhaiyan M, Thangaraju M (2007) Solubilization of zinc compounds by the diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus. Chemosphere 66:1794–1798PubMedGoogle Scholar
  113. Sardi P, Saracchi M, Quaroni S, Petrolini B, Borgonovi GE, Merli S (1992) Isolation of endophytic Streptomyces strains from surface-sterilized roots. Appl Environ Microbiol 58:2691–2693PubMedGoogle Scholar
  114. Sayer JA, Gadd GM (2001) Binding of cobalt and zinc by organic acids and culture filtrates of Aspergillus niger grown in the absence or presence of insoluble cobalt or zinc phosphate. Mycol Res 105:1261–1267Google Scholar
  115. Schelert J, Dixit V, Hoang V, Simbahan J, Drozda M, Blum P (2004) Occurrence and characterization of mercury resistance in the hyperthermophilic archaeon Sulfolobus solfataricus by use of gene disruption. J Bacteriol 186:427–437PubMedGoogle Scholar
  116. Schluenzen F, Takemoto C, Wilson DN, Kaminishi T, Harms JM, Hanawa-Suetsugu K, Szaflarski W, Kawazoe M, Shirouzo M, Nierhaus KH, Yokoyama S, Fucini P (2006) The antibiotic kasugamycin mimics mRNA nucleotides to destabilize tRNA binding and inhibit canonical translation initiation. Nat Struct Mol Biol 13:871–886PubMedGoogle Scholar
  117. Schmidt A, Haferburg G, Sineriz M, Merten D, Buchel G, Kothe E (2005) Heavy metal resistance mechanisms in actinobacteria for survival in AMD contaminated soils. Chem Erd Geochem 65:131–144Google Scholar
  118. Schutze E, Weist A, Klose M, Wach T, Schumann M, Nietzsche S, Merten D, Baumert J, Majzlan J, Kothe E (2013) Taking nature into lab: biomineralization by heavy metal resistant Streptomycetes in soil. Biogeosciences 10:2345–2375Google Scholar
  119. Sharma A, Johri BN (2003) Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS9 in maize (Zea mays L.) under iron limiting conditions. Microbiol Res 158:243–248PubMedGoogle Scholar
  120. Sheng X, He L, Wang Q, Ye H, Jiang C (2008) Effects of inoculation of biosurfactant-producing bacillus sp. J119 on plant growth and cadmium uptake in a cadmium-amended soil. J Hazard Mater 155:17–22PubMedGoogle Scholar
  121. Sikora RA, Schafer K, Dababat AA (2007) Modes of action associated with microbially induced in planta suppression of plant-parasitic nematodes. Australas Plant Pathol 36:124–134Google Scholar
  122. Silver S (1998) Genes for all metals—a bacterial view of the periodic table The 1996 Thom Award lecture. J Ind Microbiol Biotechnol 20:1–12PubMedGoogle Scholar
  123. Silver S, Phung LT (1996) Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol 50:753–890PubMedGoogle Scholar
  124. Sineriz M, Kothe E, Abate CM (2009) Cadmium biosorption by Streptomyces sp. F4 isolated from former uranium mine. J Basic Microbiol 49:55–62Google Scholar
  125. Solano BR, Barriuso J, Gutierrez Manero FJ (2008) Physiological and molecular mechanisms of plant growth promoting rhizobacteria (PGPR). In: Ahmad I, Pichtel J, Hayat S (eds) Plant-bacteria interactions strategies and techniques to promote plant growth. Wiley, Weinheim, pp 41–54Google Scholar
  126. Solans M (2007) Discaria trinervis-Frankia symbiosis promotion by saprophytic actinomycetes. J Basic Microbiol 47:243–250PubMedGoogle Scholar
  127. Solans M, Vobis G, Cassan F, Luna V, Wall LG (2011) Production of phytohormones by root-associated saprophytic actinomycetes isolated from the actinorhizal plant Ochetophila trinervis. World J Microbiol Biotechnol 27:2195–2202Google Scholar
  128. Sriprang R, Hayashi M, Ono H, Takagi M, Hirata K, Murooka Y (2003) Enhanced accumulation of Cd2+ by a Mesorhizobium sp. transformed with a gene from Arabidopsis thaliana coding for phytochelatin synthase. Appl Environ Microbiol 69:1791–1796PubMedGoogle Scholar
  129. Stolz JF, Basu P, Santini JM, Oremland RS (2006) Arsenic and selenium in microbial metabolism. Annu Rev Microbiol 60:107–130PubMedGoogle Scholar
  130. Stolz JF, Basu P, Oremland RS (2010) Microbial arsenic metabolism: new twists on an old poison. Microbe 5:53–59Google Scholar
  131. Tipayno S, Chang-Gi K, Sa T (2012) T-RFLP analysis of structural changes in soil bacterial communities in response to metal and metalloid contamination and initial phytoremediation. Appl Soil Ecol 61:137–146Google Scholar
  132. Trivedi P, Pandey A, Sa T (2007) Chromate reducing and plant growth promoting activities of psychrotrophic Rhodococcus erythropolis MtCC7905. J Basic Microbiol 47:513–517PubMedGoogle Scholar
  133. Umrania VV (2006) Bioremediation of toxic heavy metals using acidothermophilic autotrophies. Bioresour Technol 97:1237–1242PubMedGoogle Scholar
  134. Valls M, Lorenzo DV (2002) Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol Rev 26:327–338PubMedGoogle Scholar
  135. Valls M, Atrian S, Lorenzo DV, Fernandez LA (2000) Engineering a mouse metallothionein on the cell surface of Ralstonia eutropha CH34 for immobilization of heavy metals in soil. Nat Biotechnol 18:661–665PubMedGoogle Scholar
  136. Van Der Lelie D, Corbisier P, Diels L, Gilis A, Lodewyckx C, Mergeay M, Taghavi S, Spelmans N, Vangronsveld J (2000) The role of bacteria in the phytoremediation of heavy metals. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. CRC Press, Boca Raton, pp 265–281Google Scholar
  137. Venkatesh NM, Vedaraman M (2012) Remediation of soil contaminated with copper using rhamnolipids produced from Pseudomonas aeruginosa MTCC 2297 using waste frying rice bran oil. Ann Microbiol 62:85–91Google Scholar
  138. Wang Q, Kim D, Dionysiou DD, Sorial GA, Timberlake D (2004) Source and remediation for mercury contamination in aquatic systems—a literature review. Environ Pollut 131:323–336PubMedGoogle Scholar
  139. Wheeler CT, Hughes LT, Oldroyd J, Pulford ID (2001) Effect of nickel on Frankia and its symbiosis with Alnus glutinosa (L.) gaertn. Plant Soil 231:81–90Google Scholar
  140. Wolfe-Simon F, Blum JS, Kulp TR, Gordon GW, Hoeft SE, Ridge JP, Stolz JF, Webb SM, Weber PK, Davies PCW, Anbar AD, Oremland RS (2011) A bacterium that can grow by using arsenic instead of phosphorus. Science 332:1163–1166PubMedGoogle Scholar
  141. Wu SC, Luo YM, Cheung KC, Wong MH (2006) Influence of bacteria on Pb and Zn speciation, mobility and bioavailability in soil: a laboratory study. Environ Pollut 144:765–773PubMedGoogle Scholar
  142. Wu SC, Peng XL, Cheung KC, Liu SL, Wong MH (2009) Adsorption kinetics of Pb and Cd by two plant growth promoting rhizobacteria. Bioresour Technol 100:4559–4563PubMedGoogle Scholar
  143. Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Seifeddine Ben Tekaya
    • 1
  • Sherlyn Tipayno
    • 1
  • Kiyoon Kim
    • 1
  • Parthiban Subramanian
    • 1
  • Tongmin Sa
    • 1
  1. 1.Department of Environmental and Biological ChemistryChungbuk National UniversityCheongjuRepublic of Korea

Personalised recommendations