Advertisement

Geosciences Journal

, Volume 22, Issue 3, pp 423–432 | Cite as

Impact of Shewanella oneidensis on heavy metals remobilization under reductive conditions in soil of Guilan Province, Iran

  • Nasrin Ghorbanzadeh
  • Rahul Kumar
  • Sang-hun Lee
  • Hyun-Sung Park
  • Byong-Hun Jeon
Article

Abstract

Remobilization of heavy metals in contaminated soil due to anaerobic bioreduction by Shewanella oneidensis was studied. Glucose and anthraquinone-2,6-disulphonate (AQDS) were used as an electron donor and an electron shuttle, respectively. The bioreduction caused a gradual increase in dissolved Mn(II) concentration upto 15 days followed by stationary state. The aqueous Fe(II) concentration increased and reached a highest level on the 10th day, followed by a slight decrease before the steady state was reached. The concentration of Cu(II) was at its extreme level on 5th day and then decreased before reaching the steady state. The highest dissolution was observed for Zn(II) on the 10th day followed by a decrease upto 25th day. Enhanced reduction of Fe(III) and mobilization of selected heavy metals were observed in the presence of S. oneidensis and AQDS. The soluble and acid-extractable Fe(II) concentration was higher in the presence of glucose. The remobilization efficiencies of Mn(II), Fe(II), Cu(II), and Zn(II) were 41%, 48%, 53%, and 63%, respectively. After bioreduction, Fe(II)/Cu(II) and Mn(II)/Zn(II) posed moderate and high risks, respectively. The results of this study will be useful to highlight the effects of variable redox conditions on the bioreduction process to determine the bioavailability of heavy metals in soil.

Key words

anaerobic conditions Shewanella oneidensis iron oxyhydroxide remobilization reductive dissolution 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Antić-Mladenović, S., Rinklebe, J., Frohne, T., Strak, H., Wennrich, R., Tomic, Z., and Licina, V., 2011, Impact of controlled redox conditions on nickel in a serpentine soil. Journal of Soils and Sediments, 11, 406–415.CrossRefGoogle Scholar
  2. ASTM D422, 2007, Standard test method for particle-size analysis of soil. American Society for Testing and Materials International, West Conshohocken, 2–7p. DOI: 10.1520/D0422-63R07E02Google Scholar
  3. Ayyasamy, P.M., Chun, S., and Lee, S., 2009, Desorption and dissolution of heavy metals from contaminated soil using Shewanella sp. (HN-41) amended with various carbon sources and synthetic soil organic matters. Journal of Hazardous Materials, 161, 1095–1102.Google Scholar
  4. Bao, S.D., 2005, Soil Agricultural Chemistry Analysis. China Agriculture Press, Beijing, 270 p.Google Scholar
  5. Bose, S., Hochella, M.F.J., Gorby, Y.A., Kennedy, D.W., McCready, D.E., Madden, A.S., and Lower, B.H., 2009, Bio-reduction of hematite nanoparticles by the dissimilatory iron reducing bacterium Shewanella oneidensis MR-1. Geochimica et Cosmochimica Acta, 73, 962–976.CrossRefGoogle Scholar
  6. Brookshaw, D.R., Lloyd, J.R., Vaughan, D.J., and Pattrick, A.D.R., 2014, Bioreduction of biotite and chlorite by a Shewanella species. American Mineralogist, 99, 1746–1754.CrossRefGoogle Scholar
  7. Coby, A.J. and Picardal, F.W., 2006, Influence of sediment components on the immobilization of Zn during microbial Fe-(hydr)oxide reduction. Environmental Science and Technology, 40, 3813–3818.CrossRefGoogle Scholar
  8. Cooper, D.C., Picardal, F., Rivera, J., and Talbot, C., 2000, Zinc immobilization and magnetite formation via ferric oxide reduction by Shewanella putrefaciens. Environmental Science and Technology, 34, 100–106.CrossRefGoogle Scholar
  9. Cooper, D.C., Picardal, F.F., and Coby, A.J., 2006, Interactions between microbial iron reduction and metal geochemistry: Effect of redox cycling on transition metal speciation in iron bearing sediments. Environmental Science and Technology, 40, 1884–1891.CrossRefGoogle Scholar
  10. Davranche, M. and Bollinger, J.C., 2000, Heavy metals desorption from synthesized and natural iron and manganese oxyhydroxides: effect of reductive conditions. Colloid and Interface Science, 227, 531–539.CrossRefGoogle Scholar
  11. Davranche, M. and Bollinger, J.C., 2001, A desorption-dissolution model for metal release from polluted soil under reductive conditions. Journal of Environmental Quality, 30, 1581–1586.CrossRefGoogle Scholar
  12. Dong, H., Kukkadapu, R., Fredrickson, J.K., Zachara, J.M., Kennedy, D.W., and Kostandarithes, H.M., 2003a, Microbial reduction of structural Fe(III) in illite and goethite. Environmental Science and Technology, 37, 1268–1276.Google Scholar
  13. Dong, H., Kostka, J.E., and Kim, J.W., 2003b, Microscopic evidence for microbial dissolution of smectite. Clays and Clay Minerals, 51, 502–512.Google Scholar
  14. Dong, H., Jaisi, D.P., Kim, J., and Zhang, G., 2009, Microbe-clay mineral interactions. American Mineralogist, 94, 1505–1519.CrossRefGoogle Scholar
  15. EPA-ROC, 1994, The standard methods for determination of heavy metals in soils and plants. National Institute of Environmental Analysis of EPA-ROC, Taipei, p. 5–8.Google Scholar
  16. Fu, B., Zhou, H., Zhang, R., and Qiu, G., 2008, Bioleaching of chalcopyrite by pure and mixed cultures of Acidithiobacillus spp. and Leptospirillum ferriphilum. International Biodeterioration and Biodegradation, 62, 109–115.CrossRefGoogle Scholar
  17. Fu, L., Li, S.W., Ding, Z.W., Ding, J., Lu, Y.Z., and Zeng, R.J., 2016, Iron reduction in the DAMO/Shewanella oneidensis MR-1 coculture system and the fate of Fe(II). Water Research, 88, 808–815.CrossRefGoogle Scholar
  18. Ghrefat, H. and Yusuf, N., 2006, Assessing Mn, Fe, Cu, Zn, and Cd pollution in bottom sediments of Wadi Al-Arab Dam, Jordan. Chemosphere, 65, 2114–2121.CrossRefGoogle Scholar
  19. Han, H.J. and Lee, J.U., 2015, Experimental study on bioleaching of paddy soil in the vicinity of refinery site contaminated with copper, lead, and arsenic using sulfur-oxidizing bacteria. Geosystem Engineering, 18, 79–84.CrossRefGoogle Scholar
  20. Horváth, B., Opara-Nadi, O., and Beese, F., 2005, A simple method for measuring the carbonate content of soils. Soil Science Society of America journal, 69, 1066–1068.CrossRefGoogle Scholar
  21. Hu, C., Zhang, Y., Zhang, L., and Luo, W., 2014, Effects of microbial iron reduction and oxidation on the immobilization and mobilization of copper in synthesized Fe(III) minerals and Fe-rich soils. Journal of Microbiology and Biotechnology, 24, 534–544.CrossRefGoogle Scholar
  22. Ikem, A. and Adisa, S., 2011, Runoff effect on eutrophic lake water quality and heavy metal distribution in recent littoral sediment. Chemosphere, 82, 259–267.CrossRefGoogle Scholar
  23. Inglett, P.W., Reddy, K.R., and Corstanje, R., 2005, Anaerobic soils. In: Hillel, D. and Hatfield, J.L. (eds.), Encyclopedia of Soils in the Environment. Elsevier, Amsterdam, p. 72–78.CrossRefGoogle Scholar
  24. Jain, C.K., 2004, Metal fractionation study on bed sediments of River Yamuna, India. Water Research, 38, 569–578.CrossRefGoogle Scholar
  25. Jaradat, Q.M., Massadeh, A.M., Zaitoun, M.A., and Maitah, B.M., 2006, Fractionation and sequential extraction of heavy metals in the soil of scrapyard of discarded vehicles. Environmental Monitoring and Assessment, 112, 197–210.CrossRefGoogle Scholar
  26. Kabala, C. and Sing, B.R., 2001, Fractionation and mobility of copper, lead, and zinc in soil profiles in the vicinity of a copper smelter. Journal of Environmental Quality, 30, 485–492.CrossRefGoogle Scholar
  27. Kim, J.W., Dong, H., Seabaugh, J., Newell, S.W., and Eberl, D.D., 2004, Role of microbes in the smectite-to-illite reaction. Science, 303, 830–832.CrossRefGoogle Scholar
  28. Kim, J.W., Furukawa, Y., Dong, H., and Newell, S.W., 2005, The role of microbial Fe(III) reduction in the clay flocculation. Clays and Clay Minerals, 53, 572–579.CrossRefGoogle Scholar
  29. Kostka, J.E., Dalton, D.D., Skelton, H., Dollhopf, S., and Stucki, J.W., 2002, Growth of iron(III)-reducing bacteria on clay minerals as the sole electron acceptor and comparison of growth yields on a variety of oxidized iron forms. Applied and Environmental Microbiology, 68, 6256–6262.CrossRefGoogle Scholar
  30. Lee, E.Y., Noh, S.R., Cho, K.S., and Ryu, H.W., 2001, Leaching of Mn, Co, and Ni from manganese nodules using an anaerobic bioleaching method. Journal of Bioscience and Bioengineering, 92, 354–359.CrossRefGoogle Scholar
  31. Lee, J.H., Roh, Y., and Hur, H.G., 2008, Microbial production and characterization of super paramagnetic magnetite nanoparticles by Shewanella sp. HN-41. Journal of Microbiology and Biotechnology, 18, 1572–1577.Google Scholar
  32. Li, X., Shen, Z., Wai, O.W.H., and Li, Y.S., 2001, Chemical forms of Pb, Zn and Cu in the sediment profiles of the Pearl River Estuary. Marine Pollution Bulletin, 42, 215–223.CrossRefGoogle Scholar
  33. Liu, G., Qiu, S., Liu, B., Pu, Y., Gao, Z., Wang, J., Jin, R., and Zhou, J., 2017, Microbial reduction of Fe(III)-bearing clay minerals in the presence of humic acids. Scientific Reports, 7, 45354.CrossRefGoogle Scholar
  34. MacDonald, L.H., Moon, H.S., and Jaffe, P.R., 2011, The role of biomass, electron shuttles, and ferrous iron in the kinetics of Geobacter sulfurreducens mediated ferrihydrite reduction. Water Research, 45, 1049–1062.CrossRefGoogle Scholar
  35. Ma, L.Q. and Dong, Y., 2004, Effects of incubation on solubility and mobility of trace metals in two contaminated soils. Environmental Pollution, 130, 301–307.CrossRefGoogle Scholar
  36. Mescouto, C.S.T., Lemos, V.P., Dantas Filho, H.A., da Costa, M.L., Kern, D.C., and Fernandes, K.G., 2011, Distribution and availability of copper, iron, manganese and zinc in the archaeological black earth profile from the amazon region. Journal of the Brazilian Chemical Society, 22, 1484–1492.Google Scholar
  37. Muehe, E.M., Adaktylou, I.J., Obst, M., Zeitvogel, F., Behrens, S., Planer-Friedrich, B., Kraemer, U., and Kappler, A., 2013, Organic carbon and reducing conditions lead to cadmium immobilization by secondary Fe mineral formation in a pH-neutral soil. Environmental Science and Technology, 47, 13430–13439.CrossRefGoogle Scholar
  38. Nguyen, V.K., Lee, M.H., Park, H.J., and Lee, J.U., 2015, Bioleaching of arsenic and heavy metals from mine tailings by pure and mixed cultures of Acidithiobacillus spp. Journal of Industrial and Engineering Chemistry, 21, 451–458.CrossRefGoogle Scholar
  39. Opuene, K. and Agbozu, I.E., 2008, Relationships between heavy metals in shrimp (Macrobrachium felicinum) and metal levels in the water column and sediments of Taylor Creek. International Journal of Environmental Research, 2, 343–348.Google Scholar
  40. O’Reilly, S.E., Furukawa, Y., and Newell, S., 2006, Dissolution and microbial Fe(III) reduction of nontronite (NAu-1). Chemical Geology, 235, 1–11.CrossRefGoogle Scholar
  41. Parmar, N., 2001, Formation of green rust and immobilization of nickel in response to bacterial reduction of hydrous ferric oxide. Geomicrobiology Journal, 18, 375–385.CrossRefGoogle Scholar
  42. Piepenbrock, A., Dippon, U., Porsch, K., Appel, E., and Kappler, A., 2011, Dependence of microbial magnetite formation on humic substance and ferrihydrite concentrations. Geochimica et Cosmochimica Acta, 75, 6844–6858.CrossRefGoogle Scholar
  43. Rodríguez, L., Ruiz, E., Alonso-Azcáratec, J., and Rincón, J., 2009, Heavy metal distribution and chemical speciation in tailings and soils around a Pb-Zn mine in Spain. Journal of Environmental Management, 90, 1106–1116.CrossRefGoogle Scholar
  44. Sipos, P., Choi, C., Németh, T., Szalai, Z., and Póka, T., 2014, Relationship between iron and trace metal fractionation in soils. Chemical Speciation and Bioavailability, 26, 21–30.CrossRefGoogle Scholar
  45. Stookey, L.I., 1970, Ferrozine–a new spectrophotometric regent for iron. Analytical Chemistry, 42, 779–781.CrossRefGoogle Scholar
  46. Sundaray, S.K., Nayak, B.B., Lin, S., and Bhatta, D., 2011, Geochemical speciation and risk assessment of heavy metals in the river estuarine sediments–a case study: Mahanadi basin, India. Journal of Hazardous Materials, 186, 1837–1846.CrossRefGoogle Scholar
  47. Tessier, A., Campbell, P.G.C., and Bisson, M., 1979, Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry, 51, 844–851.CrossRefGoogle Scholar
  48. Vaxevanidou, K., Giannikou, S., and Papassiopi, N., 2012, Microbial arsenic reduction in polluted and unpolluted soils from Attica, Greece. Journal of Hazardous Materials, 241–242, 307–315.CrossRefGoogle Scholar
  49. Vaxevanidou, K., Papassiopi, N., and Paspaliaris, I., 2008, Removal of heavy metals and arsenic from contaminated soils using bioremediation and chelant extraction techniques. Chemosphere, 70, 1329–1337.CrossRefGoogle Scholar
  50. Veglio, F., 1996, The optimization of manganese dioxide bioleaching media by fractional factorial experiments. Process Biochemistry, 31, 773–785.CrossRefGoogle Scholar
  51. Vink, J.P.M., Harmsen, J., and Rijnaarts, H., 2010, Delayed immobilization of heavy metals in soils and sediments under reducing and anaerobic conditions: consequences for flooding and storage. Journal of Soils and Sediments, 10, 1633–1645.CrossRefGoogle Scholar
  52. Walkley, A. and Black, A.I., 1934, Examination of the Degtjareff method for determining soil organic matter and a proposed modification of the chromic and titration method. Soil Science, 34, 29–38.CrossRefGoogle Scholar
  53. Wang, F. and Tessier, A., 2009a, Zero-valent sulfur and metal speciation in sediment pore waters of freshwater lakes. Environmental Science and Technology, 43, 7252–7257.CrossRefGoogle Scholar
  54. Wang, X.J., Chen, X.P., Yang, J., Wang, Z.S., and Sun, G.X., 2009b, Effect of microbial mediated iron plaque reduction on arsenic mobility in paddy soil. Journal of Environmental Sciences, 21, 1562–1568.CrossRefGoogle Scholar
  55. Zachara, J.M., Fredrickson, J.K., Smith, S.C., and Gassman, P.L., 2001, Solubilization of Fe(III) oxide-bound trace metals by a dissimilatory Fe(III) reducing bacterium. Geochimica et Cosmochimica Acta, 65, 75–93.CrossRefGoogle Scholar
  56. Zhang, M., Dale, J.R., DiChristina, T.J., and Stack, A.G., 2009, Dissolution morphology of iron (oxy)(hydr)oxides exposed to the dissimilatory iron-reducing bacterium Shewanella oneidensis MR-1. Geomicrobiology Journal, 26, 83–92.CrossRefGoogle Scholar
  57. Zhang, M.K., Liu, Z.Y., and Wang, H., 2010, Use of single extraction methods to predict bioavailability of heavy metals in polluted soils to rice. Communications in Soil Science and Plant Analysis, 41, 820–831.CrossRefGoogle Scholar
  58. Zhang, Y., Hu, C., and Luo, W., 2014, Influences of electron donor, bicarbonate, and sulfate on bio-reduction processes and manganese/ copper redistributions among minerals in a water-saturated sediment. Soil and Sediment Contamination, 23, 94–106.CrossRefGoogle Scholar

Copyright information

© The Association of Korean Geoscience Societies and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Nasrin Ghorbanzadeh
    • 1
  • Rahul Kumar
    • 2
  • Sang-hun Lee
    • 3
  • Hyun-Sung Park
    • 4
  • Byong-Hun Jeon
    • 2
    • 5
  1. 1.Department of Soil Science, Faculty of Agricultural SciencesUniversity of GuilanRashtIran
  2. 2.Department of Earth Resources and Environmental EngineeringHanyang UniversitySeoulRepublic of Korea
  3. 3.Department of Environmental ScienceKeimyung UniversityDaeguRepublic of Korea
  4. 4.Mine Reclamation CorporationWonjuRepublic of Korea
  5. 5.Department of Earth Resources and Environmental EngineeringHanyang UniversitySeoulRepublic of Korea

Personalised recommendations