Microbial reduction of Fe(III) in smectite minerals by thermophilic methanogen Methanothermobacter thermautotrophicus

Geochimica et Cosmochimica Acta

Volumn 106, Issue , 2013, Pages 203-215

  Zhang, Jing ^a,b   Dong, Hailiang ^a,b   Liu, Deng ^c   Agrawal, Abinash ^d  

^a CHINA UNIVERSITY OF GEOSCIENCES   (China)

^b MIAMI UNIVERSITY   (United States)

^c CHINA UNIVERSITY OF GEOSCIENCES   (China)

^d WRIGHT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANOXIC CONDITIONS; IRON; METHANOGENESIS; METHANOGENIC BACTERIUM; MICROBIAL ACTIVITY; MONTMORILLONITE; REDUCTION; SMECTITE; THERMOPHILIC BACTERIUM;

METHANOTHERMOBACTER THERMAUTOTROPHICUS;

EID: 84873470022     PISSN: 00167037     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gca.2012.12.031     Document Type: Article

References (68)

1. Abken H.J., Tietze M., Brodersen J., Bäumer S., Beifuss U., Deppenmeier U. Isolation and characterization of methnophenazine and function of phenazines in membrane-bound elevtron transport of Methanosarcina mazei Gö1. J. Bacteriol. 1998, 180:2027-2032.
2. Achtnich C., Bak F., Conrad R. Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol. Fertil. Soils 1995, 19:65-72.
3. Adams M.W.W. Biochemical diversity among sulfur-dependent, hyperthermophilic microorganisms. FEMS Microbiol. Rev. 1994, 15:261-277.
4. Amonette J.E., Templeton J.C. Improvements to the quantitative assay of nonrefractory minerals for Fe(II) and total Fe using 1,10-phenanthroline. Clays Clay Miner. 1998, 46(1):51-62.
5. Aplin A.C., Matenaar I.F., McCarty D.K., van der Pluijm B.A. Influence of mechanical compaction and clay mineral diagenesis on the microfabric and porescale properties of deepwater Gulf of Mexico mudstones. Clays Clay Miner. 2006, 54:500-514.
6. Arnold R.G., DiChristina T.J., Hoffmann M.R. Inhibitor studies of dissimilative Fe(III) reduction by Pseudomonas sp. strain 200 (" Pseudomonas ferrireductans" ). Appl. Environ. Microbiol. 1986, 52:281-289.
7. Atreya S.K., Mahaffy P.R., Wong A.S. Methane and related trace species on Mars: Origin, loss, implications for life, and habitability. Planet. Space Sci. 2007, 55:358-369.
8. Baross J.A., Hoffman S.E. Submarine hydrothermal vents and associated gradient environments as sites for the origin and evolution of life. Origins Life 1985, 15:327-345.
9. Bishop M.E., Dong H., Kukkadapu R.K., Edelmann R.E. Bioreduction of Fe-bearing clay minerals and their reactivity toward pertechnetate (Tc-99). Geochim. Cosmochim. Acta 2011, 75:5229-5246.
10. Bock G.R., Goode J.A. Evolution of Hydrothermal Ecosystems on Earth (and Mars?) 1996, Wiley, West Sussex, England.
11. Bond D.R., Lovley D.R. Reduction of Fe(III) oxide by methanogens in the presence and absence of extracellular quinones. Environ. Microbiol. 2002, 4(2):115-124.
12. Canfield D.E., Kristensen E., Thamdrup B. Aquatic Geomicrobiology, Advances in Marine Biology 2005, vol. 48. Elsevier, Oxford, United Kingdom.
13. Chapelle H.F., O'Neill K., Bradley M.P., Methe A.B., Clufo A.S., Knobel L.L., Lovley R.D. A hydrogen-based subsurface microbial community dominated by methanogens. Nature 2002, 415:312-315.
14. Chastain K.B., Kral A.T. Approaching Mars-like geochemical conditions in the laboratory: Omission of artificial buffers and reductants in a study of biogenic methane production on a smectite clay. Astrobiology 2010, 10:889-897.
15. Chidthaisong A., Conrad R. Turnover of glucose and acetate coupled to reduction of nitrate, ferric iron, and to methanogenesis in anoxic field soil. FEMS Microbiol. Ecol. 2000, 31:73-86.
16. Deppenmeier U., Lienard T., Gottschalk G. Novel reactions involved in energy conservation by methanogenic archaea. FEBS Lett. 1999, 457:291-297.
17. Dong H. Mineral transformations associated with clay-microbe interactions and implications for environmental remediation. Elements 2012, 8(2):113-118.
18. Dong H., Kukkadapu R.K., Fredrickson J.K., Zachara J.M., Kennedy D.W., Kostandarithes H.M. Microbial reduction of structural Fe(III) in illite and goethite. Environ. Sci. Technol. 2003, 37:1268-1276.
19. Dong H., Jaisi D.P., Kim J.W., Zhang G. Microbe-clay mineral interactions. Am. Mineral. 2009, 94(11-12):1505-1519.
20. Ehlmann B.L., Mustard J.F., Murchie S.L., Bibring J.P., Meunier A., Fraeman A.A., Langevin Y. Sursurface water and clay mineral formation during the early history of Mars. Nature 2011, 479:53-60.
21. Favre F., Tessier D., Abdelmoula M., Genin J.M., Gates W.P., Boivin P. Iron reduction and changes in cation exchange capacity in intermittently waterlogged soil. Eur. J. Soil Sci. 2002, 53:175-183.
22. Fetzer S., Conrad R. Effect of redox potential on methanogenesis by Methanosarcina barkeri. Arch. Microbiol. 1993, 160:108-113.
23. Frenzel P., Bosse U., Janssen P.H. Rice roots and methanogenesis in a paddy soil: Ferric iron as an alternative electron acceptor in the rooted soil. Soil Biol. Biochem. 1999, 31:421-430.
24. Gates W.P., Stucki J.W., Kirkpatrick R.J. Structural properties of reduced Upton montmorillonite. Phys. Chem. Miner. 1996, 23:535-541.
25. Gates W.P., Slade P.G., Manceau A., Lanson B. Site occupancies by iron in nontronites. Clays Clay Miner. 2002, 50:223-239.
26. Holm N.G. Why are hydrothermal systems proposed as plausible environments for the origin of life?. Origins Life Evol. Biosphere 1992, 22:5-14.
27. Jaisi D.P., Kukkadapu R.K., Eberl D.D., Dong H. Control of Fe(III) site occupancy on the rate and extent of microbial reduction of Fe(III) in nontronite. Geochim. Cosmochim. Acta 2005, 69:5429-5440.
28. Jaisi D.P., Dong H., Kim J.W., He Z., Morton J.P. Nontronite particle aggregation induced by microbial Fe(III) reduction and exopolysaccharide production. Clays Clay Miner. 2007, 55:96-107.
29. Jaisi D.P., Dong H., Liu C. Influence of biogenic Fe(II) on the extent of microbial reduction of Fe(III) in clay minerals nontronite, illite, and chlorite. Geochim. Cosmochim. Acta 2007, 71:1145-1158.
30. Jaisi D.P., Eberl D.D., Dong H. The formation of illite from nontronite by mesophilic and thermophilic bacterial reaction. Clays Clay Miner. 2011, 59:21-33.
31. Kashefi K., Lovley D.R. Extending the upper temperature limit for life. Science 2003, 301:934.
32. Kashefi K., Holmes E.D., Reysenbach A.L., Lovley R.D. Use of Fe(III) as an electron acceptor to recover previously uncultured hyperthermophiles: Isolation and characterization of Geothermobacterium ferrireducens gen., nov., sp. nov. Appl. Environ. Microbiol. 2002, 68:1735-1742.
33. Kashefi K., Tor M.J., Holmes E.D., Gaw Van Praagh C., Reysenbach A.L., Lovley R.D. Geoglobus ahangari, gen. nov., sp. nov., a novel hyperthermophilic archaeon capable of oxidizing organic acids and growing autotrophically on hydrogen with Fe(III) serving as the sole electron acceptor. Int. J. Syst. Evol. Microbiol. 2002, 52:719-728.
34. Kashefi K., Shelobolina E.S., Elliott W.C., Lovley D.R. Growth of thermophilic and hyperthermophilic Fe (III)-reducing microorganisms on a ferruginous smectite as the sole electron acceptor. Appl. Environ. Microbiol. 2008, 74:251-258.
35. Keeling J.L., Raven M.D., Gates W.P. Geology and characterization of two hydrothermal nontronites from weathered metamorphic rocks at the Uley graphite mine, South Australia. Clays Clay Miner. 2000, 48:537-548.
36. Kenealy W., Zeikus J.G. Influence of corrinoid antagonists on methanogen metabolism. J. Bacteriol. 1981, 146:133-140.
37. Kim J.W., Dong H., Seabaugh J., Newell S.W., Eberl D.D. Role of microbes in the smectite-to-illite reaction. Science 2004, 303:830-832.
38. Kostka J.E., Stucki J.W., Nealson K.H., Wu J. Reduction of structural Fe(III) in smectite by a pure culture of Shewanella putrefaciens strain MR-1. Clays Clay Miner. 1996, 44:522-529.
39. Lee K., Kostka J.E., Stucki J.W. Comparisons of structural iron reduction in smectites by bacteria and dithionite: An infrared spectroscopic study. Clays Clay Miner. 2006, 54:197-210.
40. Li Y.L., Vali H., Sears S.K., Yang J., Deng B., Zhang C.L. Iron reduction and alteration of nontronite NAu-2 by a sulfate-reducing bacterium. Geochim. Cosmochim. Acta 2004, 68(15):3251-3260.
41. Liu D., Dong H., Bishop M.E., Wang H., Agrawal A., Tritschler S., Eberl D.D., Xie S. Reduction of structural Fe(III) in nontronite by methanogen Methanosarcina barkeri. Geochim. Cosmochim. Acta 2011, 75:1057-1071.
42. Liu D., Dong H., Bishop M.E., Zhang J., Wang H., Xie S., Wang S., Huang L., Eberl D.D. Microbial reduction of structural iron in interstratified illite-smectite minerals by a sulfate-reducing bacterium. Geobiology 2012, 10:150-162.
43. Lovley D.R. Fe(III) and Mn(IV) reduction. Environmental Microbe-Metal Interactions 2000, 3-30. ASM Press, Washington, DC. D.R. Lovley (Ed.).
44. Lovley D.R., Phillips E.J.P. Competitive mechanisms for inhibition of sulfate reduction and methane production in the zone of ferric iron reduction in sediments. Appl. Environ. Microbiol. 1987, 53:2636-2641.
45. Lovley D.R., Philips E.J.P. Novel mode of microbial energy metabolism: Organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 1988, 54:1472-1480.
46. Lovley D.R., Fraga J.L., Blunt-Harris E.L., Hayes L.A., Phillips E.J.P., Coates J.D. Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydrochim. Hydrobiol. 1998, 26(3):152-157.
47. T. Int. J. Syst. Bacteriol. 1991, 41:267-274.
48. Moore D.M., Reynolds R.C. X-ray diffraction and the identification and analysis of clay minerals 1997, vols. Ch. 1, 2, & 3. Oxford University Press, New York.
49. Myers C.R., Nealson K.H. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 1988, 240(4857):1319-1321.
50. Neumann A., Petit S., Hofstetter B.T. Evaluation of redox-active iron sites in smectites using middle and near infrared spectroscopy. Geochim. Cosmochim. Acta 2011, 75:2336-2355.
51. O'Loughlin E.J., Gorski C.A., Scherer M.M., Boyanov M.I., Kemner K.M. Effects of oxyanions, natural organic matter, and bacterial cell numbers on the bioreduction of lepidocrocite (γ-FEOOH) and the formation of secondary mineralization products. Environ. Sci. Technol. 2010, 44:4570-4576.
52. Pace N.R. Origin of life-Facing up to the physical setting. Cell 1991, 65:531-533.
53. Poulet F., Bibring J.P., Mustard J.F., Gendrin A., Mangold N., Langevin Y., Arvidson R.E., Gondet B., Gomez C., Omega T. Phyllosilicates on Mars and implications for early martian climate. Nature 2005, 438:623-627.
54. Rainey A.F., Oren A. Extremophile microorganisms and the methods to handle them. Methods Microbiol. 2006, 35:1-25.
55. Reiche M., Torburg G., Küsel K. Competition of Fe(III) reduction and methanogenesis in an acidic fen. FEMS Microbiol. Ecol. 2008, 65:88-101.
56. Roden E.E., Wetzel R.G. Organic carbon oxidation and suppression of methane production by microbial Fe(III) oxide reduction in vegetated and unvegetated freshwater wetland sediments. Limnol. Oceanogr. 1996, 41:1733-1748.
57. Roden E.E., Wetzel R.G. Competition between Fe(III)-reducing and methanogenic bacteria for acetate in iron-rich freshwater sediments. Microb. Ecol. 2003, 45:252-258.
58. Schwarzenbach R.P., Gschwend P.M., Imboden D.M. Environmental Organic Chemistry, Illustrative Examples, Problems, and Case Studies 1995, John Wiley and Sons, Inc., New York.
59. Stucki J.W., Komadel P., Wilkinson H.T. Microbial reduction of structural iron(III) in smectites. Soil Sci. Soc. Am. J. 1987, 51:1663-1665.
60. Stucki J.W., Kostka J.E. Microbial reduction of iron in smectite. C. R. Geosci. 2006, 338:468-475.
61. van Bodegom P.M., Stams A.J.M. Influence of alternative electron acceptors on methanogenesis in rice paddy soils. Chemosphere 1999, 39:167-182.
62. van Bodegom P.M., Scholten J.C.M., Stams A.J.M. Direct inhibition of methanogenesis by ferric iron. FEMS Microbiol. Ecol. 2004, 49:261-268.
63. Vargas M., Kashefi K., Blunt-Harris E.L., Lovley D.R. Microbiological evidence for Fe(III) reduction on early Earth. Nature 1998, 395:65-67.
64. Yao H., Conrad R. Thermodynamics of methane production in different rice paddy soils from China, the Philippines, and Italy. Soil Biol. Biochem. 1999, 31:463-473.
65. Zehnder A.J.B., Wuhermann K. Physiology of a Methanobacterium strain AZ. Arch. Microbiol. 1977, 111:199-205.
66. 3+ in nontronite by a thermophilic bacterium and its role in promting the smectite to illite reaction. Am. Mineral. 2007, 92:1411-1419.
67. Zhang G., Kim J.W., Dong H., Sommer A.J. Microbial effects in promoting the smectite to illite reaction: Role of organic matter intercalated in the interlayer. Am. Mineral. 2007, 92:1401-1410.
68. Zhang J., Dong H., Liu D., Fischer B.T., Wang S., Huang L. Microbial reduction of Fe(III) in illite-smectite minerals by methanogen Methanosarcina mazei. Chem. Geol. 2012, 292-293:35-44.