The effect of sulfate concentration on (sub)millimeter-scale sulfide δ34S in hypersaline cyanobacterial mats over the diurnal cycle

Geochimica et Cosmochimica Acta

Volumn 73, Issue 20, 2009, Pages 6187-6204

  Fike, David A ^a,b   Finke, Niko ^c,d   Zha, Jessica ^e   Blake, Garrett ^f   Hoehler, Tori M ^c   Orphan, Victoria J ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c NASA AMES RESEARCH CENTER   (United States)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f PITZER COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOGEOCHEMICAL CYCLE; CYANOBACTERIUM; DIURNAL VARIATION; HYDROGEN SULFIDE; HYPERSALINE ENVIRONMENT; ISOTOPIC COMPOSITION; ISOTOPIC FRACTIONATION; METABOLISM; MICROBIAL ACTIVITY; SULFATE-REDUCING BACTERIUM; SULFUR ISOTOPE;

BAJA CALIFORNIA SUR; GUERRERO NEGRO; MEXICO [NORTH AMERICA]; NORTH AMERICA;

CYANOBACTERIA;

EID: 69849103778     PISSN: 00167037     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gca.2009.07.006     Document Type: Article

References (106)

1. Arnosti C., Jorgensen B.B., Sagemann J., and Thamdrup B. Temperature dependence of microbial degradation of organic matter in marine sediments: polysaccharide hydrolysis, oxygen consumption, and sulfate reduction. Mar. Ecol. Prog. Ser. 165 (1998) 59-70
2. Bak F., and Cypionka H. A novel type of energy-metabolism involving fermentation of inorganic sulfur-compounds. Nature 326 (1987) 891-892
3. Baumgartner L.K., Reid R.P., Dupraz C., Decho A.W., Buckley D.H., Spear J.R., Przekop K.M., and Visscher P.T. Sulfate reducing bacteria in microbial mats: changing paradigms, new discoveries. Sedimentary Geol. 185 (2006) 131-145
4. Bebout B.M., Carpenter S.P., Des Marais D.J., Discipulo M., Embaye T., Garcia-Pichel F., Hoehler T.M., Hogan M., Jahnke L.L., Keller R.M., Miller S.R., Prufert-Bebout L.E., Raleigh C., Rothrock M., and Turk K. Long-term manipulations of intact microbial mat communities in a greenhouse collaboratory: simulating Earth's present and past field environments. Astrobiology 2 (2002) 383-402
5. Bebout B.M., Hoehler T.M., Thamdrup B., Albert D., Carpenter S., Hogan M., Turk K., and Des Marais D.J. Methane production by microbial mats under low sulphate concentrations. Geobiology 2 (2004) 87-96
6. 2. Geochim. Cosmochim. Acta 70 (2006) 5653-5664
7. Brennan S.T., Lowenstein T.K., and Horita J. Seawater chemistry and the advent of biocalcification. Geology 32 (2004) 473-476
8. Canfield D.E. Biogeochemistry of sulfur isotopes. Rev. Mineral. Geochem. Stable Isotope Geochem. 43 (2001) 607-636
9. Canfield D.E. Isotope fractionation by natural populations of sulfate-reducing bacteria. Geochim. Cosmochim. Acta 65 (2001) 1117-1124
10. Canfield D.E., and Des Marais D.J. Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochim. Cosmochim. Acta 57 (1993) 3971-3984
11. Canfield D.E., Habicht K.S., and Thamdrup B. The Archean sulfur cycle and the early history of atmospheric oxygen. Science 288 (2000) 658-661
12. Canfield D.E., Olesen C.A., and Cox R.P. Temperature and its control of isotope fractionation by a sulfate-reducing bacterium. Geochim. Cosmochim. Acta 70 (2006) 548-561
13. Canfield D.E., and Teske A. Late proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 382 (1996) 127-132
14. Canfield D.E., and Thamdrup B. The production of S-34-depleted sulfide during bacterial disproportionation of elemental sulfur. Science 266 (1994) 1973-1975
15. Canfield D.E., Thamdrup B., and Fleischer S. Isotope fractionation and sulfur metabolism by pure and enrichment cultures of elemental sulfur-disproportionating bacteria. Limnol. Oceanogr. 43 (1998) 253-264
16. Castenholz R.W., Jorgensen B.B., Damelio E., and Bauld J. Photosynthetic and behavioral versatility of the cyanobacterium Oscillatoria-Boryana in a sulfide-rich microbial mat. FEMS Microbiol. Ecol. 86 (1991) 43-58
17. Chambers L.A., Trudinger P.A., Smith J.W., and Burns M.S. Fractionation of sulfur isotopes by continuous cultures of Desulfovibrio desulfuricans. Can. J. Microbiol. 21 (1975) 1602-1607
18. Claypool G.E., Holser W.T., Kaplan I.R., Sakai H., and Zak I. The age curves of sulfur and oxygen isotopes in marine sulfate and their mutual interpretation. Chem. Geol. 28 (1980) 199-260
19. Cohen Y. Comparative N and S cycles: oxygenic photosynthesis, anoxygenic photosynthesis, and sulfate-reduction in cyanobacterial mats. In: Klug M.J., and Reddy C.A. (Eds). Recent Advances in Microbial Ecology (1984), American Society for Microbiology Press, Washington D.C.
20. Cohen Y. and Helman Y. (1997) Two-dimensional sub-millimetric mapping of sulfate reduction in marine sediments. Am. Soc. Microbiol. 97th General Meeting, Abstr. 393.
21. Cohen Y., Jorgensen B.B., Padan E., and Shilo M. Sulfide-dependent anoxygenic photosynthesis in a cyanobacterium Oscillatoria Limnetica. Nature 257 (1975) 489-492
22. Cohen Y., Jorgensen B.B., Revsbech N.P., and Poplawski R. Adaption to hydrogen-sulfide of oxygenic and anoxygenic photosynthesis among cyanobacteria. Appl. Environ. Microbiol. 51 (1986) 398-407
23. Cypionka H., Smock A.M., and Bottcher M.E. A combined pathway of sulfur compound disproportionation in Desulfovivrio desulfuricans. FEMS Microbiol. Lett. 166 (1998) 181-186
24. Dannenberg S., Kroder M., Dilling W., and Cypionka H. Oxidation of H-2, organic-compounds and inorganic sulfur-compounds coupled to reduction of O-2 or nitrate by sulfate-reducing bacteria. Arch. Microbiol. 158 (1992) 93-99
25. de Wit R., and van Gemerden H. Oxidation of sulfide to thiosulfate by Microcoleus chtonoplastes. FEMS Microbiol. Lett. 45 (1987) 7-13
26. Decker K.L.M., Potter C.S., Bebout B.M., Des Marais D.J., Carpenter S., Discipulo M., Hoehler T.M., Miller S.R., Thamdrup B., Turk K.A., and Visscher P.T. Mathematical simulation of the diel O, S, and C biogeochemistry of a hypersaline microbial mat. FEMS Microbiol. Ecol. 52 (2005) 377-395
27. Des Marais D.J., Cohen Y., Nguyen H., Cheatham M., Cheatham T., and Munos E. Carbon isotopic trends in the hypersaline ponds and microbial mats at Guerrero Negro, Baja California Sur, Mexico: implications for Precambrian stromatolites. In: Cohen Y., and Rosenberg E. (Eds). Microbial Mats: Physiological Ecology of Benthic Microbial Communities (1989), American Society for Microbiology, Washington D.C.
28. Detmers J., Bruchert V., Habicht K.S., and Kuever J. Diversity of sulfur isotope fractionations by sulfate-reducing prokaryotes. Appl. Environ. Microbiol. 67 (2001) 888-894
29. Devereux R., Kane M.D., Winfrey J., and Stahl D.A. Genus- and group-specific hybridization probes for determinative and environmental studies of sulfate-reducing bacteria. Syst. Appl. Microbiol. 15 (1992) 601-609
30. Dillon J.G., Fishbain S., Miller S.R., Bebout B.M., Habicht K.S., Webb S.M., and Stahl D.A. High rates of sulfate reduction in a low-sulfate hot spring microbial mat are driven by a low level of diversity of sulfate-respiring microorganisms. Appl. Environ. Microbiol. 73 (2007) 5218-5226
31. Farquhar J., Johnston D.T., Wing B.A., Habicht K.S., Canfield D.E., Airieau S., and Thiemens M.H. Multiple sulphur isotopic interpretations of biosynthetic pathways: implications for biological signatures in the sulphur isotope record. Geobiology 1 (2003) 27-36
32. Fike D.A., Gammon C.L., Ziebis W., and Orphan V.J. Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-FISH approach. ISME J. 2 (2008) 749-759
33. 34S approach to understanding the evolution of the Ediacaran-Cambrian sulfur cycle. Geochim. Cosmochim. Acta 72 (2008) 2636-2648
34. Fike D.A., Grotzinger J.P., Pratt L.M., and Summons R.E. Oxidation of the Ediacaran ocean. Nature 444 (2006) 744-747
35. Finke N., and Jorgensen B.B. Response of fermentation and sulfate reduction to experimental temperature changes in temperate and Arctic marine sediments. ISME J. 2 (2008) 815-829
36. Finster K., Liesack W., and Thamdrup B. Elemental sulfur and thiosulfate disproportionation by Desulfocapsa sulfoexigens sp. nov., a new anaerobic bacterium isolated from marine surface sediment. Appl. Environ. Microbiol. 64 (1998) 119-125
37. Fourcans A., Ranchou-Peyruse A., Caumette P., and Duran R. Molecular analysis of the spatio-temporal distribution of sulfate-reducing bacteria (SRB) in Camargue (France) hypersaline microbial mat. Microb. Ecol. 56 (2008) 90-100
38. Fourcans A., Sole A., Diestra E., Ranchou-Peyruse A., Esteve I., Caumette P., and Duran R. Vertical migration of phototrophic bacterial populations in a hypersaline microbial mat from Salins-de-Giraud (Camargue, France). FEMS Microbiol. Ecol. 57 (2006) 367-377
39. Frund C., and Cohen Y. Diurnal cycles of sulfate reduction under oxic conditions in cyanobacterial mats. Appl. Environ. Microbiol. 58 (1992) 70-77
40. Fry B., Cox J., Gest H., and Hayes J.M. Discrimination between S-34 and S-32 during bacterial metabolism of inorganic sulfur-compounds. J. Bacteriol. 165 (1986) 328-330
41. Fry B., Gest H., and Hayes J.M. Isotope effects associated with the anaerobic oxidation of sulfide by the purple photosynthetic bacterium, Chromatium Vinosum. FEMS Microbiol. Lett. 22 (1984) 283-287
42. Fry B., Gest H., and Hayes J.M. Isotope effects associated with the anaerobic oxidation of sulfite and thiosulfate by the photosynthetic bacterium Chromatium vinosum. FEMS Microbiol. Lett. 27 (1985) 227-232
43. 2S. Chem. Geol. 58 (1986) 253-258
44. Fry B., Gest H., and Hayes J.M. S-34/S-32 fractionation in sulfur cycles catalyzed by anaerobic bacteria. Appl. Environ. Microbiol. 54 (1988) 250-256
45. Fry B., Ruf W., Gest H., and Hayes J.M. Sulfur isotope effects associated with oxidation of sulfide by O-2 in aqueous solution. Chem. Geol. 73 (1988) 205-210
46. Fukui M., Teske A., Aßmus B., Muyzer G., and Widdel F. Physiology, phylogenetic relationships, and ecology of filamentous sulfate-reducing bacteria (genus Desulfonema). Arch. Microbiol. 172 (1999) 193-203
47. Fuseler K., and Cypionka H. Elemental sulfur as an intermediate of sulfide oxidation with oxygen by Desulfobulbus proprionicus. Arch. Microbiol. 164 (1995) 104-109
48. Fuseler K., Krekeler D., Sydow U., and Cypionka H. A common pathway of sulfide oxidation by sulfate-reducing bacteria. FEMS Microbiol. Lett. 144 (1996) 129-134
49. Garrels R. M. and Lerman A. (1981). Phanerozoic cycles of sedimentary carbon and sulfur. Proc. Natl. Acad. Sci. USA 78.
50. Gill B.C., Lyons T.W., and Saltzman M.R. Parallel, high-resolution carbon and sulfur isotope records of the evolving Paleozoic marine sulfur reservoir. Palaeogeogr. Palaeocl. 256 (2007) 156-173
51. Green S.J., Blackford C., Bucki P., Jahnke L.L., and Prufert-Bebout L. A salinity and sulfate manipulation of hypersaline microbial mats reveals stasis in the cyanobacterial community structure. ISME J. 2 (2008) 457-470
52. Habicht K. S. and Canfield D. E. (1996) Sulphur isotope fractionation in modern microbial mats and the evolution of the sulphur cycle. Nature 382.
53. Habicht K.S., and Canfield D.E. Sulfur isotope fractionation during bacterial sulfate reduction in organic-rich sediments. Geochim. Cosmochim. Acta 61 (1997) 5351-5361
54. Habicht K.S., Canfield D.E., and Rethmeier J. Sulfur isotope fractionation during bacterial reduction and disproportionation of thiosulfate and sulfite. Geochim. Cosmochim. Acta 62 (1998) 2585-2595
55. Habicht K.S., Gade M., Thamdrup B., Berg P., and Canfield D.E. Calibration of sulfate levels in the Archean ocean. Science 298 (2002) 2372-2374
56. Halverson G.P., and Hurtgen M.T. Ediacaran growth of the marine sulfate reservoir. Earth Planet. Sci. Lett. 263 (2007) 32-44
57. Harrison A.G., and Thode H.G. Mechanisms of the bacterial reduction of sulfate from isotope fractionation studies. Trans. Faraday Soc. 54 (1958) 84-92
58. Hinck S., Neu T.R., Lavik G., Mussmann M., de Beer D., and Jonkers H.M. Physiological adaptation of a nitrate-storing Beggiatoa sp. to diel cycling in a phototrophic hypersaline mat. Appl. Environ. Microbiol. 73 (2007) 7013-7022
59. 2 cycling in sedimentary and phototrophic ecosystems. Antonie van Leeuwenhoek 81 (2002) 575-585
60. Hoehler T.M., Bebout B.M., and Des Marais D.J. The role of microbial mats in the production of reduced gases on the early Earth. Nature 412 (2001) 324-327
61. Hoek J., Reysenback A.-L., Habicht K.S., and 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 70 (2006) 5831-5841
62. Holser W.T. Catastrophic chemical events in history of ocean. Nature 267 (1977) 403-408
63. Holser W.T., and Kaplan I.R. Isotope geochemistry of sedimentary sulfates. Chem. Geol. 1 (1966) 93-135
64. Holser W.T., Schidlowski M., Mackenzie F.T., and Maynard J.B. Geochemical cycles of carbon and sulfur. In: Gregor C.B., Garrels R.M., MacKenzie F.T., and Maynard J.B. (Eds). Chemical Cycles in the Evolution of the Earth (1988), John Wiley & Sons, New York
65. Hurtgen M.T., Arthur M.A., and Halverson G.P. Neoproterozoic sulfur isotopes, the evolution of microbial sulfur species, and the burial efficiency of sulfide as sedimentary pyrite. Geology 33 (2005) 41-44
66. Hurtgen M.T., Arthur M.A., Prave A.R., Amend J.P.e., Edwards K.J.e., and Lyons T.W.e. The sulfur isotope composition of carbonate-associated sulfate in Mesoproterozoic to Neoproterozoic carbonates from Death Valley, California. Sulfur Biogeochem. Past Present 379 (2004) 177-194
67. Hurtgen M.T., Pruss S.B., and Knoll A.H. Evaluating the relationship between the carbon and sulfur cycles in later Cambrian ocean: an example from the Port au Port Group, western Newfoundland, Canada. Earth Planet. Sci. Lett. 281 (2009) 288-297
68. Jahnke L.L., Orphan V.J., Embaye T., Turk K.A., Kubo M., Summons R.E., and Des Marais D.J. Lipid biomarker and phylogenetic analyses to reveal archaeal biodiversity and distribution in a hypersaline microbial mat and underlying sediment. Geobiology 6 (2008) 394-410
69. Johnston D.T., Farquhar J., Wing B.A., Kaufman A.J., Canfield D.E., and Habicht K.S. Multiple sulfur isotope fractionations in biological systems: a case study with sulfate reducers and sulfur disproportionators. Am. J. Sci. 305 (2005) 645-660
70. Jorgensen B.B. A thiosulfate shunt in the sulfur cycle of marine sediments. Science 249 (1990) 152-154
71. Jorgensen B.B. Sulfate reduction and thiosulfate transformations in a cyanobacterial mat during a diel oxygen cycle. FEMS Microbiol. Ecol. 13 (1994) 303-312
72. Jorgensen B.B., Cohen Y., and Revsbech N.P. Transition from anoxygenic to oxygenic photosynthesis in a Microcoleus chthonoplastes cyanobacterial mat. Appl. Environ. Microbiol. 51 (1986) 408-417
73. Jorgensen B.B., and Des Marais D.J. Competition for sulfide among colorless and purple sulfur bacteria in cyanobacterial mats. FEMS Microbiol. Ecol. 38 (1986) 179-196
74. Jorgensen B.B., and Des Marais D.J. The diffusive boundary-layer of sediments - oxygen microgradients over a microbial mat. Limnol. Oceanogr. 35 (1990) 1343-1355
75. Kampschulte A., and Strauss H. The sulfur isotopic evolution of Phanerozoic seawater based on the analysis of structurally substituted sulfate in carbonates. Chem. Geol. 204 (2004) 255-286
76. Kaplan I.R., and Rittenberg S.C. Microbiological fractionation of sulphur isotopes. J. Gen. Microbiol. 34 (1964) 195-212
77. Kemp A. L. W. and Thode H. G. (1968) Mechanism of bacterial reduction of sulphate and of sulphite from isotope fractionation studies. Geochim. Cosmochim. Acta 32, 71
78. Krekeler D., Sigalevich P., Teske A., Cypionka H., and Cohen Y. A sulfate-reducing bacterium from the oxic layer of a microbial mat from Solar Lake (Sinai), Desulfovibrio oxyclinae sp. nov. Arch. Microbiol. 167 (1997) 369-375
79. Krekeler D., Teske A., and Cypionka H. Strategies of sulfate-reducing bacteria to escape oxygen stress in a cyanobacterial mat. FEMS Microbiol. Ecol. 25 (1998) 89-96
80. Kunin V., Raes J., Harris J.K., Spear J.R., Walker J.J., Ivanova N., von Mering C., Bebout B.M., Pace N.R., Bork P., and Hugenholtz P. Millimeter-scale genetic gradients and community-level molecular convergence in a hypersaline microbial mat. Mol. Syst. Biol. 4 (2008) 198
81. Ley R.E., Harris J.K., Wilcox J., Spear J.R., Miller S.R., Bebout B.M., Maresca J.A., Bryant D.A., Sogin M.L., and Pace N.R. Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl. Environ. Microbiol. 72 (2006) 3685-3695
82. Manz W., Eisernbrecher M., Neu T.R., and Szewzyk U. Abundance and spatial organization of Gram-negative sulfate-reducing bacteria in activated sludge investigated by in situ probing with specific 16S rRNA targeted oligonucleotides. FEMS Microbiol. Ecol. 25 (1998) 43-61
83. Minz D., Fishbain S., Green S.J., Muyzer G., Cohen Y., Rittmann B.E., and Stahl D.A. Unexpected population distribution in a microbial mat community: sulfate-reducing bacteria localized to the highly oxic chemocline in contrast to a eukaryotic preference for anoxia. Appl. Environ. Microbiol. 65 (1999) 4659-4665
84. Minz D., Flax J.L., Green S.J., Muyzer G., Cohen Y., Wagner M., Rittmann B.E., and Stahl D.A. Diversity of sulfate-reducing bacteria in oxic and anoxic regions of a microbial mat characterized by comparative analysis of dissimilatory sulfite reductase genes. Appl. Environ. Microbiol. 65 (1999) 4666-4671
85. Orphan V.J., Jahnke L.L., Embaye T., Turk K.A., Pernthaler A., Summons R.E., and Des Marais D.J. Characterization and spatial distribution of methanogens and methanogenic biosignatures in hypersaline microbial mats of Baja California. Geobiology 6 (2008) 376-393
86. Pernthaler A., Pernthaler J., and Amann R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68 (2002) 3094-3101
87. Porter D., Roychoudhury A.N., and Cowan D. Dissimilatory sulfate reduction in hypersaline coastal pans: activity across a salinity gradient. Geochim. Cosmochim. Acta 71 (2007) 5102-5116
88. Rees C.E. Steady-state model for sulfur isotope fractionation in bacterial reduction processes. Geochim. Cosmochim. Acta 37 (1973) 1141-1162
89. 2S, and pH profiles of a microbial mat. Limnol. Oceanogr. 28 (1983) 1062-1074
90. Risatti J.B., Capman W.C., and Stahl D.A. Community structure of a microbial mat: the phylogenetic dimension. Proc. Natl. Acad. Sci. 91 (1994) 10173-10177
91. Robertson C. E., Spear J. R., Harris J. K. and Pace N. R. (2009) Diversity and stratification of archaea in a hypersaline microbial mat. Appl. Environ. Microbiol. 75.
92. Ross G.M., Bloch J.D., and Krouse H.R. Neoproterozoic strata of the southern Canadian Cordillera and the isotopic evolution of seawater sulfate. Precambrian Res. 73 (1995) 71-99
93. Sagemann J., Jorgensen B.B., and Greeff O. Temperature dependence and rates of sulfate reduction in cold sediments of Svalbard, Arctic Ocean. Geomicrobiol. J. 15 (1998) 85-100
94. Sigalevich P., Baev M.V., Teske A., and Cohen Y. Sulfate reduction and possible aerobic metabolism of the sulfate-reducing bacterium Desulfovibrio oxyclinae in a chemostat coculture with Marinobacter sp strain MB under exposure to increasing oxygen concentrations. Appl. Environ. Microbiol. 66 (2000) 5005-5012
95. Spear J.R., Ley R.E., Berger A.B., and Pace N.R. Complexity in natural microbial ecosystems: the Guerrero Negro experience. Biol. Bull. 204 (2003) 168-173
96. Teske A., Ramsing N.B., Habicht K., Fukui M., Kuver J., Jorgensen B.B., and Cohen Y. Sulfate-reducing bacteria and their activities in cyanobacterial mats of Solar Lake (Sinai, Egypt). Appl. Environ. Microbiol. 64 (1998) 2943-2951
97. Thode H.D., and Monster J. Sulfur-Isotope Geochemistry of Petroleum, Evaporites, and Ancient Seas, Fluids in Subsurfaces Environments, Memoir 4 (1965), American Association of Petroleum Geologists, Tulsa, OK
98. Thode H.G. Sulfur isotope ratios in late and early Precambrian sediments and their implications regarding early environments and early life. Orig. Life Evol. Biosph. 10 (1980) 127-136
99. Visscher P.T., Baumgartner L.K., Buckley D.H., Rogers D.R., Hogan M.E., Raleigh C.D., Turk K.A., and Des Marais D.J. Dimethyl sulphide and methanethiol formation in microbial mats: potential pathways for biogenic signatures. Environ. Microbiol. 5 (2003) 296-308
100. Visscher P.T., Prins R.A., and Vangemerden H. Rates of sulfate reduction and thiosulfate consumption in a marine microbial mat. FEMS Microbiol. Ecol. 86 (1992) 283-293
101. Visscher P.T., Reid R.P., and Bebout B.M. Microscale observations of sulfate reduction: correlation of microbial activity with lithified micritic laminae in modern marine stromatolites. Geology 28 (2000) 919-922
102. Watanabe Y., Farquhar J., and Ohmoto H. Anomalous fractionations of sulfur isotopes during thermochemical sulfate reduction. Science 324 (2009) 370-373
103. Werne J.P., Lyons T.W., Hollander D.J., Formolo M.J., and Damste J.S.S. Reduced sulfur in euxinic sediments of the Cariaco Basin: sulfur isotope constraints on organic sulfur formation. Chem. Geol. 195 (2003) 159-179
104. Wieland A., de Beer D., Damgaard L.R., Kuehl M., van Dusschoten D., and Van As H. Fine-scale measurement of diffusivity in a microbial mat with nuclear magnetic resonance imaging. Limnol. Oceanogr. 46 (2001) 248-259
105. Wieringa E.B.A., Overmann J., and Cypionka H. Detection of abundant sulphate-reducing bacteria in marine oxic sediment layers by a combined cultivation and molecular approach. Environ. Microbiol. 2 (2000) 417-427
106. Wortmann U.G., Bernasconi S.M., and Boettcher M.E. Hypersulfidic deep biosphere indicates extreme sulfur isotope fractionation during single step microbial sulfate reduction. Geology 29 (2001) 647-650