Korean Journal of Soil Science and Fertilizer (한국토양비료학회지)

Korean Society of Soil Science and Fertilizer (한국토양비료학회)
권호 표지
DOI QR코드

DOI QR Code

Exploring the Potential of Bacteria-Assisted Phytoremediation of Arsenic-Contaminated Soils

  • Shagol, Charlotte C. (Department of Agricultural Chemistry, Chungbuk National University) ;
  • Chauhan, Puneet S. (Department of Agricultural Chemistry, Chungbuk National University) ;
  • Kim, Ki-Yoon (Department of Agricultural Chemistry, Chungbuk National University) ;
  • Lee, Sun-Mi (Department of Agricultural Chemistry, Chungbuk National University) ;
  • Chung, Jong-Bae (Division of Life and Environmental Science, Daegu University) ;
  • Park, Kee-Woong (Bio-Evaluation Center, KRIBB) ;
  • Sa, Tong-Min (Department of Agricultural Chemistry, Chungbuk National University)
  • Received : 2011.01.20
  • Accepted : 2011.02.22
  • Published : 2011.02.28
Download PDF
⟨ Previous Next ⟩

Abstract

Arsenic pollution is a serious global concern which affects all life forms. Being a toxic metalloid, the continued search for appropriate technologies for its remediation is needed. Phytoremediation, the use of green plants, is not only a low cost but also an environmentally friendly approach for metal uptake and stabilization. However, its application is limited by slow plant growth which is further aggravated by the phytotoxic effect of the pollutant. Attempts to address these constraints were done by exploiting plant-microbe interactions which offers more advantages for phytoremediation. Several bacterial mechanisms that can increase the efficiency of phytoremediation of As are nitrogen fixation, phosphate solubilization, siderophore production, ACC deaminase activity and growth regulator production. Many have been reported for other metals, but few for arsenic. This mini-review attempts to present what has been done so far in exploring plants and their rhizosphere microbiota and some genetic manipulations to increase the efficiency of arsenic soil phytoremediation.

Keywords

References

  1. Antoun, H. and J. Kloepper. 2001. Plant growth promoting rhizobacteria (PGPR). p. 1477-1480. In S. Brenner and J. Miller (ed.) Encyclopedia of Genetics. Academic Press.
  2. ATSDR. 2005. CERCLA Priority List of Hazardous Substances. http://www.atsdr.cdc. gov/cercla/05list.html
  3. Atlas, R.M. and J. Philip. 2005. Bioremediation: Applied microbial solutions for real-world environmental cleanup. ASM Press, Washington, D.C., USA.
  4. Baker, A.J. 1981. Accumulators and excluders strategies in the response of plants to heavy metals. J. Plant Nutr. 3:643-654. https://doi.org/10.1080/01904168109362867
  5. Barka E.A, J. Nowak, and C. Clément. 2006. Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl. Environ. Microbiol. 72:7246-52. https://doi.org/10.1128/AEM.01047-06
  6. Bech, J., C. Poschenrieder, M. Llugany, J. Barcelo, P. Tume, F.J. Tobias, J.L. Barranzuela, and E.R. Vasquez. 1997. Arsenic and heavy metal contamination of soil and vegetation around a copper mine in Northern Peru. Sci. Total Environ. 203:83-91. https://doi.org/10.1016/S0048-9697(97)00136-8
  7. Bhattacharya, P., A.B. Mukherjee, and G. Jacks. 2002. Metal contamination at a wood preservation site: characterization and experimental studies on remediation. Sci. Total Environ. 290:168-180.
  8. Bhumbla, D.K. and R.F Keefer. 1994. Arsenic mobilization and bioavailability in soils. p. 51-82. In J.O. Nriagu (ed.) Arsenic in the environment. Part I. Cycling and characterization. John Willey & Sons, Inc., New York, USA.
  9. Butcher, D.J. 2009. Phytoremediation of arsenic: Fundamental studies, practical applications, and future prospects. Appl. Spectrosc. Rev. 44:534-551. https://doi.org/10.1080/05704920903126727
  10. Cai, Y. and L.Q. Ma. 2003. Metal tolerance, accumulation and detoxification in plants with emphasis on arsenic in terrestrial plants. p. 95-114. In Y. Cai and O. Braids (ed.) Biochemistry of environmentally important trace elements. Oxford University Press, London, UK.
  11. Cavalca, L., A. Corsini, S. Bachate, and V. Andreoni. 2010. Role of PGP arsenic-resistant bacteria in As mobilization and translocation in Helianthus annuus L. In Proceedings of the 2010 19th World Congress of Soil Science, Soil Solutions for a Changing World, Brisbane, Australia.
  12. Cavalca, L., R. Zanchi, A. Corsini, M. Colombo, C. Romagnoli, E. Canzi, and V. Andreoni. 2010. Arsenic-resistant bacteria associated with roots of the wild Cirsium arvense (L.) plant from an arsenic polluted soil, and screening of potential plant growth-promoting characteristics. Syst. Appl. Microbiol. 33:154-164. https://doi.org/10.1016/j.syapm.2010.02.004
  13. Chopra, B.K., S. Bhat, I.P Mikheenko, Z. Hu, Y. Yang, X. Luo, H. Chen, L. van Zwieten, R. McC. Lilley, and R. Zhang. 2007. The characteristics of rhizosphere microbes associated with plants in arsenic-contaminated soils from cattle dip sites. Sci. Total Environ. 378:331-342. https://doi.org/10.1016/j.scitotenv.2007.02.036
  14. Compant S., B. Reiter, A. Sessitsch, J. Nowak, C. Clement, and E.A. Barka. 2005. Endophytic colonization of Vitis vinifera L. by a plant growth-promoting bacterium, Burkholderia sp. strain PsJN. Appl. Environ. Microbiol. 71:1685-93. https://doi.org/10.1128/AEM.71.4.1685-1693.2005
  15. De Koe, T. 1994. Arsenic resistance in submediterranean Agrostis species. PhD Thesis, Vrije Universiteit, Amsterdam, The Netherlands.
  16. Dhankher, O.P., Y. Li, B.P. Rosen, J. Shi, D. Salt, J. Senecoff, N.A. Shasti, and R.B. Meagher. 2002. Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and γ-glutamylcysteine synthetase expression. Nature Biotechnol. 20:1140-1145. https://doi.org/10.1038/nbt747
  17. Dimpka, C.O., A. Svatos, P. Dabrowska, A. Schmidt, W. Boland, and E. Kothe. 2008. Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74:19-25. https://doi.org/10.1016/j.chemosphere.2008.09.079
  18. Fitz, W.J. and W.W. Wenzel. 2002. Arsenic transformations in the soil-rhizosphere-plant system: fundamentals and potential application to phytoremediation. J. Biotechnol. 99:259-278. https://doi.org/10.1016/S0168-1656(02)00218-3
  19. Francesconi, K., P. Visoottiviseth, and W. Sridokchan. 2002. Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos: a potential phytoremediator of arsenic-contaminated soils. Sci. Total Environ. 284:27-35. https://doi.org/10.1016/S0048-9697(01)00854-3
  20. Gerhardt, K.E., B.M. Greenberg, and B.R. Glick. 2006. The role of ACC deaminase in facilitating the phytoremediation of organics, metals and salt. Current Trends in Microbiology 2:61-73.
  21. Glick, B.R. 2010. Using soil bacteria to facilitate phytoremediation. Biotechnol. Adv. 28:367-374. https://doi.org/10.1016/j.biotechadv.2010.02.001
  22. Jonnalagadda, S.B. and G. Nenzou. 1997. Studies on arsenic rich mine dumps: II. The element uptake by vegetation. J. Environ. Sci. Health, Part A. 32:455-64.
  23. Kavamura, V.N. and E. Esposito. 2010. Biotechnological strategies applied to the decontamination of soils polluted with heavy metals. Biotechnol. Adv. 28:61-69. https://doi.org/10.1016/j.biotechadv.2009.09.002
  24. Kidd, P., J. Barcelo, M.P. Bernal, F. Navari-Izzo, C. Poschenrieder, S. Shilev, R. Clemente, and C. Monterroso. 2009. Trace element behaviour at the root-soil interface: Implications in phytoremediation. Environ. Exp. Bot. 67:243-259. https://doi.org/10.1016/j.envexpbot.2009.06.013
  25. Kim, J.J. 1989. Soil Pollution. p. 169-214. In K. Han et al. (ed.). Agricultural Environmental Chemistry, Dong-Hwa Technol. Pub. Co. Seoul, Korea.
  26. Kim, B.Y. 1993. Soil Pollution and Improvement Countermeasure. In Soil Management for Sustainable Agric. Kor. Soc. Soil Fert., Suwon, Korea. p. 68-98.
  27. King, D.J. A.I Doronila, C. Feenstra, A.J.M Baker, and I.E Woodrow. 2008. Phytostabilization of arsenical gold mine tailings using for Eucalyptus species: Growth, arsenic uptake and availability after five years. Sci. Total Environ. 406:35-42. https://doi.org/10.1016/j.scitotenv.2008.07.054
  28. Luo, C.L., Z.G. Shen, and X.D. Li. 2008. Plant uptake and leaching of metals during the hot EDDS-enhanced phytoextraction process. Int. J. Phytorem. 9:181-196.
  29. Ma, L.Q., K.M. Komar, C. Tu, W.H. Zhang, Y. Cai, and E.D. Kennelly. 2001. A fern that hyperaccumulates. Nature 409:579. https://doi.org/10.1038/35054664
  30. Ma, Y., M.N.V. Prasad, M. Rajkumar, and H. Freitas. 2011. Plant growth promoting rhizobacteria and endophyte accelerate phytoremediation of metalliferous soils. Biotechnol. Adv. 29:248-258. https://doi.org/10.1016/j.biotechadv.2010.12.001
  31. Mandal, B.K. and K.T. Suzuki. 2002. Arsenic round the world: a review. Talanta 58:201-235. https://doi.org/10.1016/S0039-9140(02)00268-0
  32. Mandal, S.M., B. Pati, R. Das, K. Amit, and K. A. Ghosh. 2008. Characterization of a symbiotically effective Rhizobium resistant to arsenic: Isolated from root nodules of Vigna mungo (L.) Hepper grown in arsenic-contaminated field. J. Gen. Appl. Microbiol. 54:93-99. https://doi.org/10.2323/jgam.54.93
  33. Meagher, R.B. and A.C. Heaton. 2005. Strategies for the engineered phytoremediation of toxic element pollution: mercury and arsenic. J. Ind. Microbiol. Biotechnol. 32:502-13. https://doi.org/10.1007/s10295-005-0255-9
  34. Meharg, A.A. and J. Hartley-Whitaker. 2002. Arsenic uptake and metabolism in arsenic resistant and non-resistant plant species. New Phytol. 154:29-43. https://doi.org/10.1046/j.1469-8137.2002.00363.x
  35. Merkle, S. 2005. Engineering forest trees with heavy metal resistance genes for phytoremediation. p. 117-120. In Agricultural Biotechnology: Beyond Food and Energy to Health and Environment. National Agricultural Biotechnology Council, New York, USA.
  36. Nie, L., S. Shah, A. Rashid, G.I. Burd, D.G. Dixon, and B. Glick. 2002. Phytoremediation of arsenate contaminated soil by transgenic canola and the plant growth-promoting bacterium Enterobacter cloacae CAL2. Plant Physiol. Biochem. 40:355-361. https://doi.org/10.1016/S0981-9428(02)01375-X
  37. Nordstrom, D.K. 2002. Worldwide occurrences of arsenic in ground water. Science 296:2143-2145. https://doi.org/10.1126/science.1072375
  38. Nriagu, J.O. and J.M Pacyna. 1988. Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature 333:134-139. https://doi.org/10.1038/333134a0
  39. Nriagu, J.O. 1989. A global assessment of natural sources of atmospheric trace metals. Nature (London) 338:47-49. https://doi.org/10.1038/338047a0
  40. Nriagu, J.O. 2002. Arsenic poisoning through the ages. p. 1-50. In W.T. Frankenberger (ed.) Environmental chemistry of arsenic. Marcel Dekker, New York, USA.
  41. Nriagu, J.O., P. Bhattacharya, A.B. Mukherjee, J. Bundschuh, R. Zevenhoven, and R.H. Loppert. 2007. Arsenic in soil and groundwater: an overview. p. 3-60. In P. Bhattacharya et al. (ed.) Arsenic in soil and groundwater environment. Trace Metals and Other Contaminants in the Environment, Vol. 9. Elsevier, New York, USA.
  42. O'Neill, P. 1995. Arsenic. p. 105-121. In B.J. Alloway (ed.) Heavy metals in soils. Blackie Academic and Professional, London, UK
  43. Pacyna, J.M. and E.G. Pacyna. 2001. An assessment of global and regional emissions of trace metals in the atmosphere from anthropogenic sources world. Environ. Rev. 9:269-298. https://doi.org/10.1139/a01-012
  44. Panda, S.K., R.K. Upadhyay, and S. Nath. 2010. Arsenic stress in plants. J. Agron. Crop Sci. 196:161-174 https://doi.org/10.1111/j.1439-037X.2009.00407.x
  45. Pierzynski, G.M., J.T. Sims, and G.F. Vance. 2005. Soils and environmental quality. CRC Press, Boca Raton, FL, USA.
  46. Pillay, V.K. and J. Nowak. 1997. Inoculum density, temperature, and genotype effects on in vitro growth promotion and epiphytic and endophytic colonization of tomato (Lycopersicon esculentum L.) seedlings inoculated with a pseudomonad bacterium. Can. J. Microbiol. 43:354-61. https://doi.org/10.1139/m97-049
  47. Porter, E.K. and P.J. Peterson. 1975. Arsenic accumulation by plants on mine waste (United Kingdom). Sci. Total Environ. 4:365-371. https://doi.org/10.1016/0048-9697(75)90028-5
  48. Pulford, I.D. and C. Watson. 2003. Phytoremediation of heavy metal-contaminated land by trees - A review. Environ. Int. 29:529-540. https://doi.org/10.1016/S0160-4120(02)00152-6
  49. Rajkumar, M., M.N. Vara Prasad, H. Freitas, and N. Ae. 2009. Biotechnological applications of serpentine soil bacteria for phytoremediation of trace metals. Crit. Rev. Biotechnol. 29:120-130. https://doi.org/10.1080/07388550902913772
  50. Rajkumar, M., N. Ae, M.N. Vara Prasad, and H. Freitas. 2010. Potential of siderophore-producing bacteria for improving heavy metal extraction. Trends Biotechnol. 28:142-149. https://doi.org/10.1016/j.tibtech.2009.12.002
  51. Reed, M. and B. Glick. 2005. Growth of canola (Brassica napus) in the presence of plant growth-promoting bacteria in either copper and polyaromatic hydrocarbons. Can. J. Microbiol. 51:1061-1069. https://doi.org/10.1139/w05-094
  52. Reichman, S.M. 2007. The potential of the legume-rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol. Biochem. 39:2587-2593. https://doi.org/10.1016/j.soilbio.2007.04.030
  53. Rutherford, D.W., A.J. Bednar, J.R. Garbarino, R. Needham, K.W. Staver, and R.L. Wershaw. 2003. Environmental fate of roxarsone in poultry litter. Part II. Mobility of arsenic in soils amended with poultry litter. Environ. Sci. Technol. 37:1515-1520. https://doi.org/10.1021/es026222+
  54. Ryan R.P., K. Germaine, A. Franks, D.J. Ryan, and D.N. Dowling. 2008. Bacterial endophytes: recent developments and applications. FEMS Microbiol. Lett. 278:1-9. https://doi.org/10.1111/j.1574-6968.2007.00918.x
  55. Safronova, V., V. Stepanok, G. Engqvist, Y. Alekseyev, and A. Belimov. 2006. Root associated bacteria containing 1- aminocyclopropane-1-carboxylate deaminase improve growth and nutrient uptake by pea genotypes cultivated in cadmium supplemented soil. Biol. Fertil. Soils. 42:267-272. https://doi.org/10.1007/s00374-005-0024-y
  56. Saleem, M., M. Arshad, S. Hussain, and A. Bhatti. 2007. Perspective on plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J. Ind. Microbiol. 34:635-648. https://doi.org/10.1007/s10295-007-0240-6
  57. Salt, D.E., M. Blaylock, N.P.B.A. Kumar, V. Duschenkov, B.D. Ensley, I. Chet, and I. Raskin. 1995. Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnol. 13:468-474. https://doi.org/10.1038/nbt0595-468
  58. Schulz, B. and C. Boyle. 2006. What are endophytes? p. 1-13. In Schulz B. et al. (ed.) Microbial Root Endophytes. Springer-Verlag, Berlin.
  59. Sinha, S. and S.K. Mukherjee. 2008. Cadmium-induced siderophore production by a high Cd-resistant bacterial strain relieved Cd toxicity in plants through root colonization. Curr. Microbiol. 56:55-60. https://doi.org/10.1007/s00284-007-9038-z
  60. Sizova, O.I., V.V. Kochetkov, and A.M. Boronin. 2006. The arsenic-phytoremediation potential of genetically modified Pseudomonas spp. In J.L. Morel et al. (ed.) Phytoremediation of metal-contaminated soils. Vol. 68. NATO Series. Springer, The Netherlands.
  61. Smith, S.E., H.M. Christophersen, S. Pope, and F.A. Smith. 2010. Arsenic uptake and toxicity in plants: integrating mycorrhizal influences. Plant Soil 327:1-21. https://doi.org/10.1007/s11104-009-0089-8
  62. Treeby, M., H. Marschner, and V. Romheld. 1989. Mobilization of iron and other micronutrient cations from a calcareous soil by plant borne, microbial and synthetic chelators. Plant Soil 114:217-22. https://doi.org/10.1007/BF02220801
  63. US EPA. 1999. Phytoremediation resource guide. US Environmental Protection Agency. Washington DC, USA.
  64. Vazquez, S., R. Agha, A. Granado, M.J. Sarro, E. Esteban, J.M. Penalosa, and R.O. Carpena. 2006. Use of white lupine plant for stabilization of Cd and As polluted acid soil. Water Air Soil Pollut. 177:349-365. https://doi.org/10.1007/s11270-006-9178-y
  65. Wang, S. and X. Zhao. 2009. On the potential of biological treatment for arsenic contaminated soils and groundwater. J. Environ. Manage. 90:2367-2376. https://doi.org/10.1016/j.jenvman.2009.02.001
  66. Wenzel, W.W., D.C. Adriano, D. Salt, and R. Smith. 1999. Phytoremediation: a plant-microbe-based remediation system. p. 457-508. In D.C. Adriano et al. (ed.) Agronomy Monograph 37, Madison, WI, USA.
  67. Xiong, J., L. Wu, S. Tu, J.D. Van Nostrand, Z. He, J. Zhou, and G. Wang. 2010. Microbial communities and functional genes associated with soil arsenic contamination and the rhizosphere of the arsenic-hyperaccumulating plant Pteris vittata L. Appl. Environ. Microbiol. 76:7277-7284. https://doi.org/10.1128/AEM.00500-10
  68. Yang, J.E., Y.K. Kim, J.H. Kim, and Y.H. Park. 1999. Environmental impacts and management strategies of trace metals in soil and groundwater in The Republic of Korea. p. 270-289. In P.M. Huang and I.K. Iskandar (ed.) Soils and groundwater pollution and remediation Asia, Africa, and Oceania. CRC Press, New York, USA.
  69. Zhao, F.J., S.J. Dunham, and S.P. McGrath. 2002. Arsenic hyperaccumulation by different fern species. New Phytol. 156:27-31. https://doi.org/10.1046/j.1469-8137.2002.00493.x
  70. Zhuang, X., J. Chen, H. Shim, and Z. Bai. 2007. New advances in plant growth promoting rhizobacteria for bioremediation. Environ. Int. 33:406-413. https://doi.org/10.1016/j.envint.2006.12.005

Cited by

  1. Concurrent uptake and metabolism of dyestuffs through bio-assisted phytoremediation: a symbiotic approach 2017, https://doi.org/10.1007/s11356-017-0029-8