Effects of dissimilatory sulfate reduction on FeIII (hydr)oxide reduction and microbial community development

Geochimica et Cosmochimica Acta

Volumn 129, Issue , 2014, Pages 177-190

  Kwon, Man Jae ^a,b   Boyanov, Maxim I ^a   Antonopoulos, Dionysios A ^a   Brulc, Jennifer M ^a   Johnston, Eric R ^a   Skinner, Kelly A ^a   Kemner, Kenneth M ^a   O'Loughlin, Edward J ^a  

^a ARGONNE NATIONAL LABORATORY   (United States)

^b Korea Institute of Science and Technology   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BIOGEOCHEMICAL CYCLE; BIOGEOCHEMISTRY; COMMUNITY DEVELOPMENT; COMMUNITY RESPONSE; FERRIHYDRITE; HYDROXIDE; IRON; LEPIDOCROCITE; MICROBIAL COMMUNITY; REDUCTION; SEDIMENT CHEMISTRY; SULFATE;

UNITED STATES;

EID: 84897644907     PISSN: 00167037     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gca.2013.09.037     Document Type: Article

References (88)

1. Akob D.M., Mills H.J., Gihring T.M., Kerkhof L., Stucki J.W., Anastacio A.S., Chin K.-J., Kusel K., Palumbo A.V., Watson D.B., Kostka J.E. Functional diversity and electron donor dependence of microbial populations capable of U(VI) reduction in radionuclide-contaminated subsurface sediments. Appl. Environ. Microbiol. 2008, 74:3159-3170.
2. Amirbahman A., Sigg L., Gunten U. Reductive dissolution of Fe(III) (hydr)oxides by cysteine: kinetics and mechanism. J. Colloid Interface Sci. 1997, 194:194-206.
3. Anderson R.T., Vrionis H.A., Ortiz-Bernad I., Resch C.T., Long P.E., Dayvault R., Karp K., Marutzky S., Metzler D.R., Peacock A., White D.C., Lowe M., Lovley D.R. Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl. Environ. Microbiol. 2003, 69:5884-5891.
4. Benning L.G., Wilkin R.T., Konhauser K.O. Iron monosulphide stability: experiments with sulphate reducing bacteria. Geochemistry of the Earth's Surface 1999, 429-432. A.A. Balkema, Rotterdam. H. Ármannsson (Ed.).
5. Bethke C.M., Ding D., Jin Q., Sanford R.A. Origin of microbiological zoning in groundwater flows. Geology 2008, 36:739-742.
6. Boone D.R., Bryant M.P. Propionate-degrading bacterium, Syntrophobacter wolinii sp. nov. gen. nov., from methanogenic ecosystems. Appl. Environ. Microbiol. 1980, 40:626-632.
7. Canfield D.E., Raiswell R., Bottrell S.H. The reactivity of sedimentary iron minerals toward sulfide. Am. J. Sci. 1992, 292:659-683.
8. Caporaso J.G., Bittinger K., Bushman F.D., DeSantis T.Z., Andersen G.L., Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 2010, 26:266-267.
9. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Pena A.G., Goodrich J.K., Gordon J.I., Huttley G.A., Kelley S.T., Knights D., Koenig J.E., Ley R.E., Lozupone C.A., McDonald D., Muegge B.D., Pirrung M., Reeder J., Sevinsky J.R., Turnbaugh P.J., Walters W.A., Widmann J., Yatsunenko T., Zaneveld J., Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7:335-336.
10. Chapelle F.H., Lovley D.R. Competitive exclusion of sulfate reduction by Fe(III)-reducing bacteria: a mechanism for producing discrete zones of high-iron ground water. Ground Water 1992, 30:29-36.
11. DOE U.S. (1999) Final site observational work plan for the UMTRA project Old Rifle site GJO-99-88-TAR. In Department of Energy (ed. U.S.). Grand Junction CO.
12. Donald R., Southam G. Low temperature anaerobic bacterial diagenesis of ferrous monosulfide to pyrite. Geochim. Cosmochim. Acta 1999, 63:2019-2023.
13. dos Santos Afonso M., Stumm W. Reductive dissolution of iron(III) (hydr)oxides by hydrogen sulfide. Langmuir 1992, 8:1671-1675.
14. Edgar R.C. Search and clustering orders of magnitude faster than blast. Bioinformatics 2010, 26:2460-2461.
15. Finneran K.T., Forbush H.M., VanPraagh C.V.G., Lovley D.R. Desulfitobacterium metallireducens sp. nov., an anaerobic bacterium that couples growth to the reduction of metals and humic acids as well as chlorinated compounds. Int. J. Syst. Evol. Microbiol. 2002, 52:1929-1935.
16. Fredrickson J.K., Zachara J.M., Kennedy D.W., Dong H., Onstott T.C., Hinman N.W., Li S.-m. Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium. Geochim. Cosmochim. Acta 1998, 62:3239-3257.
17. García-Balboa C., Cautivo D., Blázquez M., González F., Muñoz J., Ballester A. Successive ferric and sulphate reduction using dissimilatory bacterial cultures. Water Air Soil Pollut. 2010, 207:213-226.
18. Geets J., Borremans B., Vangronsveld J., Diels L., Lelie D. Molecular monitoring of SRB community structure and dynamics in batch experiments to examine the applicability of in situ precipitation of heavy metals for groundwater remediation (15 pp). J. Soil Sed. 2005, 5:149-163.
19. Glasauer S., Weidler P.G., Langley S., Beveridge T.J. Controls on Fe reduction and mineral formation by a subsurface bacterium. Geochim. Cosmochim. Acta 2003, 67:1277-1288.
20. Goorissen H.P., Boschker H.T.S., Stams A.J.M., Hansen T.A. Isolation of thermophilic Desulfotomaculum strains with methanol and sulfite from solfataric mud pools, and characterization of Desulfotomaculum solfataricum sp. nov. Int. J. Syst. Evol. Microbiol. 2003, 53:1223-1229.
21. Hansel C.M., Benner S.G., Fendorf S. Competing Fe(II)-induced mineralization pathways of ferrihydrite. Environ. Sci. Technol. 2005, 39:7147-7153.
22. Haveman S.A., DiDonato R.J., Villanueva L., Shelobolina E.S., Postier B.L., Xu B., Liu A., Lovley D.R. Genome-wide gene expression patterns and growth requirements suggest that Pelobacter carbinolicus reduces Fe(III) indirectly via sulfide production. Appl. Environ. Microbiol. 2008, 74:4277-4284.
23. Herbert R.B., Benner S.G., Pratt A.R., Blowes D.W. Surface chemistry and morphology of poorly crystalline iron sulfides precipitated in media containing sulfate-reducing bacteria. Chem. Geol. 1998, 144:87-97.
24. Howarth R.W., Stewart J.W.B. The interactions of sulphur with other elements cycles in ecosystems. Sulphur Cycling on the Continents: Wetlands, Terrestrial Ecosystems and Associated Water Bodies 1992, 67-84. John Wiley, Chichester. R.W. Howarth, J.W.B. Stewart, M.V. Ivanov (Eds.).
25. Isaksen M.F., Bak F., Jørgensen B.B. Thermophilic sulfate-reducing bacteria in cold marine sediment. FEMS Microbiol. Ecol. 1994, 14:1-8.
26. Jakobsen R., Postma D. Redox zoning, rates of sulfate reduction and interactions with Fe-reduction and methanogenesis in a shallow sandy aquifer, Rømø, Denmark. Geochim. Cosmochim. Acta 1999, 63:137-151.
27. Kaksonen A.H., Spring S., Schumann P., Kroppenstedt R.M., Puhakka J.A. Desulfotomaculum thermosubterraneum sp. nov., a thermophilic sulfate-reducer isolated from an underground mine located in a geothermally active area. Int. J. Syst. Evol. Microbiol. 2006, 56:2603-2608.
28. Kirk M.F., Holm T.R., Park J., Jin Q., Sanford R.A., Fouke B.W., Bethke C.M. Bacterial sulfate reduction limits natural arsenic contamination in groundwater. Geology 2004, 32:953-956.
29. Komlos J., Moon H.S., Jaffé P.R. Effect of sulfate on the simultaneous bioreduction of iron and uranium. J. Environ. Qual. 2008, 37:2058-2062.
30. Konhauser K., Riding R. Bacterial biomineralization. Fundamentals of Geobiology 2012, 105-130. John Wiley & Sons Ltd.
31. Koretsky C.M., Moore C.M., Lowe K.L., Meile C., DiChristina T.J., Van Cappellen P. Seasonal oscillation of microbial iron and sulfate reduction in saltmarsh sediments (Sapelo Island, GA, USA). Biogeochemistry 2003, 64:179-203.
32. Kostka J.E., Haefele E., Viehweger R., Stucki J.W. Respiration and dissolution of iron(III)-containing clay minerals by bacteria. Environ. Sci. Technol. 1999, 33:3127-3133.
33. Kropf A.J., Katsoudas J., Chattopadhyay S., Shibata T., Lang E.A., Zyryanov V.N., Ravel B., McIvor K., Kemner K.M., Scheckel K.G., Bare S.R., Terry J., Kelly S.D., Bunker B.A., Segre C.U. The new MRCAT (Sector 10) bending magnet beamline at the Advanced Photon Source. AIP Conf. Proc. 2010, 1234:299-302.
34. Kukkadapu R.K., Zachara J.M., Fredrickson J.K., Kennedy D.W., Dohnalkova A.C., Mccready D.E. Ferrous hydroxy carbonate is a stable transformation product of biogenic magnetite. Am. Mineral. 2005, 90:510-515.
35. Kwon M.J., Sanford R.A., Park J., Kirk M.F., Bethke C.M. Microbiological response to well pumping. Ground Water 2008, 46:286-294.
36. Laanbroek H.J., Pfennig N. Oxidation of short-chain fatty acids by sulfate-reducing bacteria in freshwater and in marine sediments. Arch. Microbiol. 1981, 128:330-335.
37. Larsen O., Postma D. Kinetics of reductive bulk dissolution of lepidocrocite, ferrihydrite, and goethite. Geochim. Cosmochim. Acta 2001, 65:1367-1379.
38. Lee S.H., Lee I., Roh Y. Biomineralization of a poorly crystalline Fe(III) oxide, akaganeite, by an anaerobic Fe(III)-reducing bacterium (Shewanella alga) isolated from marine environment. Geosci. J. 2003, 7:203-288.
39. Lefort S., Mucci A., Sundby B. Sediment response to 25 years of persistent hypoxia. Aquat. Geochem. 2012, 18:461-474.
40. Lentini C.J., Wankel S.D., Hansel C.M. Enriched iron(III)-reducing bacterial communities are shaped by carbon substrate and iron oxide mineralogy. Front. Microbiol. 2012, 3:404.
41. 2S. Geomicrobiol. J. 2006, 23:103-117.
42. Liger E., Charlet L., Van Cappellen P. Surface catalysis of uranium(VI) reduction by iron(II). Geochim. Cosmochim. Acta 1999, 63:2939-2955.
43. Lovley D.R. Dissimilatory metal reduction. Annu. Rev. Microbiol. 1993, 47:263-290.
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., Stolz J.F., Nord G.L., Phillips E.J.P. Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism. Nature 1987, 330:252-254.
46. Lovley D.R., Giovannoni S.J., White D.C., Champine J.E., Phillips E.J.P., Gorby Y.A., Goodwin S. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch. Microbiol. 1993, 159:336-344.
47. Lozupone C., Lladser M.E., Knights D., Stombaugh J., Knight R. UniFrac: an effective distance metric for microbial community comparison. ISME J. 2011, 5:169-172.
48. Lueders T., Friedrich M. Archaeal population dynamics during sequential reduction processes in rice field soil. Appl. Environ. Microbiol. 2000, 66:2732-2742.
49. Megonigal J.P., Hines M.E., Visscher P.T. Anaerobic metabolism: linkages to trace gasses and aerobic processes. Biogeochemistry 2004, 317-424. Elsevier-Pergamon, Oxford. W.H. Schlesinger (Ed.).
50. Min H., Zinder S.H. Isolation and characterization of a thermophilic sulfate-reducing bacterium Desulfotomaculum thermoacetoxidans sp. nov. Arch. Microbiol. 1990, 153:399-404.
51. Neal A.L., Techkarnjanaruk S., Dohnalkova A., McCready D., Peyton B.M., Geesey G.G. Iron sulfides and sulfur species produced at hematite surfaces in the presence of sulfate-reducing bacteria. Geochim. Cosmochim. Acta 2001, 65:223-235.
52. Nealson K.H., Saffarini D. Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annu. Rev. Microbiol. 1994, 48:311-343.
53. Nevin K.P., Lovley D.R. Potential for nonenzymatic reduction of Fe(III) via electron shuttling in subsurface sediments. Environ. Sci. Technol. 2000, 34:2472-2478.
54. Newville M. (1995) Program "AUTOBK" Version 2.61, 2.61 ed. University of Washington.
55. Nonaka H., Keresztes G., Shinoda Y., Ikenaga Y., Abe M., Naito K., Inatomi K., Furukawa K., Inui M., Yukawa H. Complete genome sequence of the dehalorespiring bacterium Desulfitobacterium hafniense Y51 and comparison with Dehalococcoides ethenogenes 195. J. Bacteriol. 2006, 188:2262-2274.
56. O'Loughlin E.J., Larese-Casanova P., Scherer M., Cook R. Green rust formation from the bioreduction of g-FeOOH (lepidocrocite): comparison of several Shewanella species. Geomicrobiol. J. 2007, 24:211-230.
57. Ona-Nguema G., Abdelmoula M., Jorand F., Benali O., Géhin A., Block J.-C., Génin J.-M.R. Iron(II, III) hydroxycarbonate green rust formation and stabilization from lepidocrocite bioreduction. Environ. Sci. Technol. 2002, 36:16-20.
58. Oyekola O.O., van Hille R.P., Harrison S.T.L. Competition between lactate oxidisers and fermenters under biosulphidogenic conditions: implications in the biological treatment of AMD. Adv. Mater. Res. 2009, 71-73:689-692.
59. Pedersen H.D., Postma D., Jakobsen R., Larsen O. Fast transformation of iron oxyhydroxides by the catalytic action of aqueous Fe(II). Geochim. Cosmochim. Acta 2005, 69:3967-3977.
60. Poulton S.W. Sulfide oxidation and iron dissolution kinetics during the reaction of dissolved sulfide with ferrihydrite. Chem. Geol. 2003, 202:79-94.
61. Poulton S.W., Krom M.D., Raiswell R. A revised scheme for the reactivity of iron (oxyhydr)oxide minerals towards dissolved sulfide. Geochim. Cosmochim. Acta 2004, 68:3703-3715.
62. Price M.N., Dehal P.S., Arkin A.P. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 2009, 26:1641-1650.
63. Pyzik A.J., Sommer S.E. Sedimentary iron monosulfides: kinetics and mechanism of formation. Geochim. Cosmochim. Acta 1981, 45:687-698.
64. Rabus R., Hansen T.A., Widdel F. Dissimilatory sulfate- and sulfur-reducing prokaryotes. The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community 2006, 659-768. Springer-Verlag, New York. M. Dworkin (Ed.).
65. Ravel B., Newville M. ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J. Synchrotron Radiat. 2005, 12:537-541.
66. Rickard D.T. The microbiological formation of iron sulfides. Stockholm Contrib. Geol. 1969, 20:49-66.
67. Robertson W.J., Bowman J.P., Franzmann P.D., Mee B.J. Desulfosporosinus meridiei sp. nov., a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwater. Int. J. Syst. Evol. Microbiol. 2001, 51:133-140.
68. Roden E.E. Fe(III) oxide reactivity toward biological versus chemical reduction. Environ. Sci. Technol. 2003, 37:1319-1324.
69. Schink B., Thompson T.E., Zeikus J.G. Characterization of Propionispira arboris gen. nov. sp. nov., a nitrogen-fixing anaerobe common to wetwoods of living trees. J. Gen. Microbiol. 1982, 128:2771-2779.
70. Schwertmann U., Cornell R.M. Iron Oxides in the Laboratory: Preparation and Characterization 2000, Wiley-VCH, Weinheim [u.a.].
71. Seeliger S., Janssen P.H., Schink B. Energetics and kinetics of lactate fermentation to acetate and propionate via methylmalonyl- CoA or acrylyl-CoA. FEMS Microbiol. Lett. 2002, 211:65-70.
72. Shelobolina E.S., VanPraagh C.G., Lovley D.R. Use of ferric and ferrous iron containing minerals for respiration by Desulfitobacterium frappieri. Geomicrobiol. J. 2003, 20:143-156.
73. Sørensen J. Reduction of ferric iron in anaerobic, marine sediment and interaction with reduction of nitrate and sulfate. Appl. Environ. Microbiol. 1982, 43:319-324.
74. Stookey L.L. Ferrozine-a new spectrophotometric reagent for iron. Anal. Chem. 1970, 42:779-781.
75. Straub K.L., Schink B. Ferrihydrite-dependent growth of Sulfurospirillum deleyianum through electron transfer via sulfur cycling. Appl. Environ. Microbiol. 2004, 70:5744-5749.
76. Suyama A., Iwakiri R., Kai K., Tokunaga T., Sera N., Furukawa K. Isolation and characterization of Desulfitobacterium sp. strain Y51 capable of efficient dehalogenation of tetrachloroethene and polychloroethanes. Biosci. Biotechnol. Biochem. 2001, 65:1474-1481.
77. Takai K., Moser D.P., DeFlaun M., Onstott T.C., Fredrickson J.K. Archaeal diversity in waters from deep South African gold mines. Appl. Environ. Microbiol. 2001, 67:5750-5760.
78. Taylor J., Parkes R.J. Identifying different populations of sulphate-reducing bacteria within marine sediment systems, using fatty acid biomarkers. J. Gen. Microbiol. 1985, 131:631-642.
79. Thamdrup B., Finster K., Hansen J.W., Bak F. Bacterial disproportionation of elemental sulfur coupled to chemical reduction of iron or manganese. Appl. Environ. Microbiol 1993, 59:101-108.
80. Thauer R.K., Jungermann K., Decker K. Energy conservation in chemotrophic anaerobic bacteria. Microbiol. Mol. Biol. Rev. 1977, 41:100-180.
81. Urrutia M.M., Roden E.E., Fredrickson J.K., Zachara J.M. Microbial and surface chemistry controls on reduction of synthetic Fe(III) oxide minerals by the dissimilatory iron-reducing bacterium Shewanella alga. Geomicrobiol. J. 1998, 15:269-291.
82. Utkin I., Woese C., Wiegel J. Isolation and characterization of Desulfitobacterium dehalogenans gen. nov., sp. nov., an anaerobic bacterium which reductively dechlorinates chlorophenolic compounds. Int. J. Syst. Bacteriol. 1994, 44:612-619.
83. Vaughan D.J., Lennie A.R. The iron sulphide minerals: their chemistry and role in nature. Sci. Prog. 1991, 75:371-388.
84. Vikesland P.J., Valentine R.L. Iron oxide surface-catalyzed oxidation of ferrous iron by monochloramine: implications of oxide type and carbonate on reactivity. Environ. Sci. Technol. 2002, 36:512-519.
85. Visser A., Beeksma I., Zee F., Stams A.J.M., Lettinga G. Anaerobic degradation of volatile fatty acids at different sulphate concentrations. Appl. Environ. Biotechnol. 1993, 40:549-556.
86. Widdel F., Pfennig N. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids II. Incomplete oxidation of propionate by Desulfobulbus propionicus gen. nov., sp. nov. Arch. Microbiol. 1982, 131:360-365.
87. Wu W.M., Hickey R.F., Zeikus J.G. Characterization of metabolic performance of methanogenic granules treating brewery wastewater: role of sulfate-reducing bacteria. Appl. Environ. Microbiol. 1991, 57:3438-3449.
88. 3+ oxides in single phase suspensions and subsurface materials. Am. Mineral. 1998, 83:1426-1443.