Microbially mediated re-oxidation of sulfide during dissimilatory sulfate reduction by Desulfobacter latus

Geochimica et Cosmochimica Acta

Volumn 75, Issue 12, 2011, Pages 3469-3485

  Eckert, T ^a,b   Brunner, B ^c   Edwards, E A ^b   Wortmann, U G ^b  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM; ENZYME ACTIVITY; ISOTOPIC FRACTIONATION; MEMBRANE; OXIDATION;

DESULFOBACTER LATUS;

EID: 79955385307     PISSN: 00167037     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gca.2011.03.034     Document Type: Article

References (75)

1. Bagarinao T. Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms. Aquat. Toxicol. 1992, 24(1-2):21-62.
2. Bakken L.R., Olsen R.A. Buoyant densities and dry-matter contents of microorganisms: conversion of a measured biovolume into biomass. Appl. Microbiol. Biotechnol. 1983, 45(4):1188-1195.
3. Berner R.A. Sedimentary pyrite formation. Am. J. Sci. 1970, 268:1-23.
4. Berner R.A. Sedimentary pyrite formation: an update. Geochim. Cosmochim. Acta 1984, 248:605-615.
5. Bolliger C., Schroth M.H., Bernasconi S.M., Kleikemper J., Zeyer J. Sulfur isotope fractionation during microbial sulfate reduction by toluene-degrading bacteria. Geochim. Cosmochim. Acta 2001, 65(19):3289-3298.
6. Brunner B., Bernasconi S.M. A revised isotope fractionation model for dissimilatory sulfate reduction in sulfate reducing bacteria. Geochim. Cosmochim. Acta 2005, 69(20):4759-4771.
7. Brunner B., Bernasconi S.M., Kleikemper J., Schroth M.H. A model for oxygen and sulfur isotope fractionation in sulfate during bacterial sulfate reduction processes. Geochim. Cosmochim. 2005, 69(20):4773-4785.
8. Canfield D.E. Isotope fractionation by natural populations of sulfate-reducing bacteria. Geochim. Cosmochim. Acta 2001, 65(7):1117-1124.
9. Canfield D.E., Farquhar J., Zerkle A.L. High isotope fractionations during sulfate reduction in a low-sulfate euxinic ocean analog. Geology 2010, 38(5):415-418.
10. Canfield D.E., Olesen C.A., Cox R.P. Temperature and its control of isotope fractionation by a sulfate-reducing bacterium. Geochim. Cosmochim. Acta 2006, 70(3):548-561.
11. Canfield D.E., Teske A. Late proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 1996, 382(6587):127-132.
12. Canfield D.E., Thamdrup B. The production of S34-depleted sulfide during bacterial disproportionation of elemental sulfur. Science 1994, 266(5193):1973-1975.
13. CIAAW (2007) Sulfur isotopic reference - δ34S values of sulfur isotopic reference materials. Technical Report, Commission on Isotopic Abundances and Atomic Weights, URL: http://www.ciaaw.org/sulfur.htm.
14. Cline J.D. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol. Oceanogr. 1969, 14(3):454-458.
15. Cypionka H. Uptake of sulfate, sulfite and thiosulfate by proton-anion symport in Desulfovibrio desulfuricans. Arch. Microbiol. 1987, 148(2):144-149.
16. Cypionka H. Characterization of sulfate transport in Desulfovibrio desulfuricans. Arch. Microbiol. 1989, 152(3):237-243.
17. Cypionka H. (1995) Solute transport and cell energetics. In Sulfate-Reducing Bacteria (ed. L.L. Barton). Plenum Press, New York, Biotechnology Handbooks, vol. 8. pp. 151-184.
18. Cypionka H., Smock A.M., Böttcher M.E. A combined pathway of sulfur compound disproportionation in Desulfovibrio desulfuricans. Microbiol. Lett. 1998, 166(2):181-186.
19. Davidson M.M., Bisher M.E., Pratt L.M., Fong J., Southam G., Pfiffner S.M., Reches Z., Onstott T.C. Sulfur isotope enrichment during maintenance metabolism in the thermophilic sulfate-reducing bacterium desulfotomaculum putei. Appl. Microbiol. Biotechnol. 2009, 75(17):5621-5630.
20. Detmers J., Brnchert V., Habicht K.S., Kuever J. Diversity of sulfur isotope fractionations by sulfate-reducing prokaryotes. Appl. Microbiol. Biotechnol. 2001, 67(2):888-894.
21. Farquhar J., Canfield D.E., Masterson A., Bao H., Johnston D. Sulfur and oxygen isotope study of sulfate reduction in experiments with natural populations from Fællestrand, Denmark. Geochim. Cosmochim. Acta 2008, 72(12):2805-2821.
22. Farquhar J., Johnston D.T., Wing B.A., Habicht K.S., Canfield D.E., Airieau S., Thiemens M.H. Multiple sulphur isotopic interpretations of biosynthetic pathways: implications for biological signatures in the sulphur isotope record. Geobiology 2003, 1(1):27-36.
23. Ferenci T. 'Growth of bacterial cultures' 50 years on: towards an uncertainty principle instead of constants in bacterial growth kinetics. Res. Microbiol. 1999, 150(7):431-438.
24. Fishman M. J. and Friedman L. C. (1989) Techniques of water-resources investigations of the united states geological survey. Laboratory Analysis: Methods for Determination of Inorganic Substances in Water and Fluvial Sediments TWRI5-A1. US Geological Survey, Reston, VA, USA.
25. Fitz R.M., Cypionka H. Formation of thiosulfate and trithionate during sulfite reduction by washed cells of desulfovibrio-desulfuricans. Arch. Microbiol. 1990, 154(4):400-406.
26. Fry J.C. Determination of biomass. Methods in Aquatic Bacteriology, Modern Microbiological Methods 1988, 27-72. Wiley, New York, (Chapter 2). B. Austin (Ed.).
27. Fukui M., Suwa Y., Urushigawa Y. High survival efficiency and ribosomal rna decaying pattern of Desulfobacter latus, a highly specific acetate-utilizing organism, during starvation. FEMS Microbiol. Ecol. 1996, 19(1):17-25.
28. Funk W., Dammann V., Donnevert G. Quality Assurance in Analytical Chemistry 2007, Wiley-VCH Verlag, Weinheim. second ed.
29. Habicht K.S., Salling L., Thamdrup B., Canfield D.E. Effect of low sulfate concentrations on lactate oxidation and isotope fractionation during sulfate reduction by Archaeoglobus fulgidus Strain Z. Appl. Microbiol. Biotechnol. 2005, 71(7):3770-3777.
30. Hadas O., Malinsky-Rushansky N., Pinkas R., Cappenberg T.E. Grazing on autotrophic and heterotrophic picoplankton by ciliates isolated from Lake Kinneret, Israel. J. Plankton. Res. 1998, 20(8):1435-1448.
31. Harrison A.G., Thode H.G. Mechanism of the bacterial reduction of sulphate from isotope fractionation studies. Trans. Faraday Soc. 1958, 54(1):84-92.
32. Hoek J., Reysenbach A.L., Habicht K.S., Canfield D.E. Effect of hydrogen limitation and temperature on the fractionation of sulfur isotopes by a deep-sea hydrothermal vent sulfate-reducing bacterium. Geochim. Cosmochim. Acta 2006, 70(23):5831-5841.
33. Hyun J.H., Yang E.J. Freezing seawater for the long-term storage of bacterial cells for microscopic enumeration. J. Microbiol. 2003, 41(3):262-265.
34. Icgen B., Harrison S. Exposure to sulfide causes populations shifts in sulfate-reducing consortia. Res. Microbiol. 2006, 157(8):784-791.
35. Isaksen M.F., Jørgensen B.B. Adaptation of psychrophilic and psychrotrophic sulfate-reducing bacteria to permanently cold marine environments. Appl. Microbiol. Biotechnol. 1996, 62(2):408-414.
36. Morgan J. J. and Stone A. T. (1985) Kinetics of chemical processes of importance in lacustrine environments. In Chemical Processes in Lakes (ed. W. Stumm). Wiley, New York. pp. 389-426 (Chapter 17).
37. Moore J. W. and Pearson R. G. (1981) Kinetics and Mechanism, third ed. Wiley, New York.
38. Johnston D.T., Farquhar J., Canfield D.E. Sulfur isotope insights into microbial sulfate reduction: when microbes meet models. Geochim. Cosmochim. Acta 2007, 71(16):3929-3947.
39. Johnston D.T., Farquhar J., Wing B.A., Kaufman A., Canfield D.E., Habicht K.S. Multiple sulfur isotope fractionations in biological systems: a case study with sulfate reducers and sulfur disproportionators. Am. J. Sci. 2005, 305(6-8):645-660.
40. Jones G.A., Pickard M.D. Effect of titanium(III) citrate as reducing agent on growth of rumen bacteria. Appl. Microbiol. Biotechnol. 1980, 39(6):1144-1147.
41. Jørgensen B.B. A theoretical model of the stable sulfur isotope distribution in marine sediments. Geochim. Cosmochim. Acta 1979, 43(3):363-374.
42. Jørgensen B.B. Bacteria and marine biogeochemistry. Marine Geochemistry 2006, 169-206. Springer, Berlin, (Chapter 5). H.D. Schulz, M. Zabel (Eds.).
43. Jørgensen B.B., Böttcher M.E., Luschen H., Neretin L.N., Volkov I. Anaerobic methane oxidation and a deep H2S sink generate isotopically heavy sulfides in black sea sediments. Geochim. Cosmochim. Acta 2004, 68(9):2095-2118.
44. Kaplan I.R., Rittenberg S.C. Microbiological fractionation of sulphur isotopes. J. Gen. Microbiol. 1964, 34(2):195-212.
45. Kemp A.L.W., Thode H.G. The mechanism of bacterial reduction of sulphate and of sulphite from isotope fractionation studies. Geochim. Cosmochim. Acta 1968, 32(1):71-91.
46. Kinoshita M., Paynter M.J.B. A self-refilling syringe for dispensing anaerobic media. Biotechnol. Tech. 1988, 2(3):159-162.
47. Knoblauch C., Jørgensen B.B. Effect of temperature on sulphate reduction, growth rate and growth yield in five psychrophilic sulphate-reducing bacteria from arctic sediments. Environ. Microbiol. 1999, 1(5):457-467.
48. CRC Handbook of Chemistry and Physics: A Ready-reference Book of Chemical and Physical Data 2006, Taylor and Francis, New York. 87th ed. D.R. Lide (Ed.).
49. Lloyd K.G., Edgcomb V.P., Molyneaux S.J., Boer S., Wirsen C.O., Atkins M.S., Teske A. Effects of dissolved sulfide, ph, and temperature on growth and survival of marine hyperthermophilic archaea. Appl. Environ. Microbiol. 2005, 71(10):6383-6387.
50. Madigan M.T. Brock Biology of Microorganisms 2006, Pearson Prentice Hall, Upper Saddle River, NJ. 11th ed.
51. Mangalo M., Einsiedl F., Meckenstock R.U., Stichler W. Influence of the enzyme dissimilatory sulfite reductase on stable isotope fractionation during sulfate reduction. Geochim. Cosmochim. Acta 2008, 72(6):1513-1520.
52. Mangalo M., Meckenstock R.U., Stichler W., Einsiedl F. Stable isotope fractionation during bacterial sulfate reduction is controlled by reoxidation of intermediates. Geochim. Cosmochim. Acta 2007, 71(17):4161-4171.
53. Mariotti A., Germon J.C., Hubert P., Kaiser P., Letolle R., Tardieux A., Tardieux P. Experimental-determination of nitrogen kinetic isotope fractionation - some principles - illustration for the denitrification and nitrification processes. Plant Soil 1981, 62(3):413-430.
54. Mayer B., Krouse H.R. Procedures for sulfur isotope abundance studies. Handbook of stable isotope analytical techniques 2004, vol. 1:538-603. Elsevier, Amsterdam, (Chapter 26).
55. Moosa S., Harrison S.T.L. Product inhibition by sulphide species on biological sulphate reduction for the treatment of acid mine drainage. Hydromet 2006, 83(1-4):214-222.
56. Okabe S., Nielsen P.H., Characklis W.G. Factors affecting microbial sulfate reduction by Desulfovibrio desulfuricans in continuous culture - limiting nutrients and sulfide concentration. Biotechnol. Bioeng. 1992, 40(6):725-734.
57. Okabe S., Nielsen P.H., Jones W.L., Characklis W.G. Sulfide product inhibition of Desulfovibrio desulfuricans in batch and continuous cultures. Water Res. 1995, 29(2):571-578.
58. Overmann J. Principles of enrichment, isolation, cultivation and preservation of prokaryotes. The Prokaryotes 2006, vol. 1:80-136. Springer, New York, (third ed., Chapter 1.5).
59. Parkhurst D. L. and Appelo C. A. J. (1999) User's guide to PHREEQC (version 2); a computer program for speciation, batch-reaction, one-dimensional transport, and inverse geochemical calculations. Water-Resources Investigations Report 99-4259. US Geological Survey, Reston, VA, USA.
60. Postgate J.R. The Sulphate-Reducing Bacteria 1984, Cambridge Univ. Press, Cambridge. second ed.
61. Rees C.E. Steady-state model for sulfur isotope fractionation in bacterial reduction processes. Geochim. Cosmochim. Acta 1973, 37(5):1141-1162.
62. Robinson J.A., Tiedje J.M. Non-linear estimation of monod growth kinetic-parameters from a single substrate depletion curve. Appl. Microbiol. Biotechnol. 1983, 45(5):1453-1458.
63. Rudnicki M.D., Elderfield H., Spiro B. Fractionation of sulfur isotopes during bacterial sulfate reduction in deep ocean sediments at elevated temperatures. Geochim. Cosmochim. Acta 2001, 65(5):777-789.
64. Scott K.M., Lu X., Cavanaugh C.M., Liu J.S. Optimal methods for estimating kinetic isotope effects from different forms of the Rayleigh distillation equation. Geochim. Cosmochim. Acta 2004, 68(3):433-442.
65. Szabo A., Tudge A., Macnamara J., Thode H.G. The distribution of S-34 in nature and the sulfur cycle. Science 1950, 111(2887):464-465.
66. Thode H.G., Kleerekoper H., McElcheran D. Isotope fractionation in the bacterial reduction of sulfate. Res. Lond. 1951, 4:581-582.
67. Trudinger P.A., Chambers L.A. Reversibility of bacterial sulfate reduction and its relevance to isotope fractionation. Geochim. Cosmochim. Acta 1973, 37(7):1775-1778.
68. Werne J.P., Lyons T.W., Hollander D.J., Formolo M.J., Damste J.S.S. Reduced sulfur in euxinic sediments of the Cariaco Basin: sulfur isotope constraints on organic sulfur formation. Chem. Geol. 2003, 195(1-4):159-179.
69. Widdel F. New types of acetate-oxidizing, sulfate-reducing Desulfobacter species, D. hydrogenophilus sp. nov., D. latus sp. nov., and D. curvatus sp. nov. Arch. Microbiol. 1987, 148(4):286-291.
70. Widdel F. Microbiology and Ecology of Sulfate- and Sulfur-Reducing Bacteria, Ecological and Applied Microbiology 1988, Wiley, New York, (Chapter 10, pp. 469-585).
71. Widdel F. and Bak F. (1992) Gram-negative mesophilic sulfate-reducing bacteria. In The Prokaryotes (eds. A. Balows, H. G. Trueper, M. Dworkin, W. Harder and K. H. Schleifer). Springer, New York, vol. 4. pp. 3352-3378 (2nd ed.).
72. Wortmann U.G., Bernasconi S.M., Böttcher M.E. Hypersulfidic deep biosphere indicates extreme sulfur isotope fractionation during single-step microbial sulfate reduction. Geology 2001, 29(7):647-650.
73. Wortmann U.G., Chernyavsky B., Bernasconi S.M., Brunner B., Böttcher M.E., Swart P.K. Oxygen isotope biogeochemistry of pore water sulfate in the deep biosphere: dominance of isotope exchange reactions with ambient water during microbial sulfate reduction (ODP Site 1130). Geochim. Cosmochim. Acta 2007, 71(17):4221-4232.
74. Wortmann U.G., Chernyavsky B.M. Effect of evaporite deposition on Early Cretaceous carbon and sulphur cycling. Nature 2007, 446(7136):654-656.
75. Zehnder A.J.B., Wuhrmann K. Titanium (III) citrate as a nontoxic oxidation-reduction buffering system for culture of obligate anaerobes. Science 1976, 194(4270):1165-1166.