Abstract
The metabolic activities of microbial mats have likely regulated biogeochemical cycling over most of Earth's history. However, the relationship between metabolic activity and the establishment of isotopic geochemical gradients in these mats remains poorly constrained. Here we present a parallel microgeochemical and microbiological study of micron-scale sulfur cycling within hypersaline microbial mats from Guerrero Negro, Baja California Sur, Mexico. Dissolved sulfide within the mats was captured on silver discs and analyzed for its abundance and δ34S isotopic composition using high-resolution secondary ion mass spectrometry (nanoSIMS). These results were compared to sulfide and oxygen microelectrode profiles. Two-dimensional microgeochemical mapping revealed well-defined laminations in sulfide concentration (on scales from 1 to 200 μm), trending toward increased sulfide concentrations at depth. Sulfide δ34S decreased from ∼+10‰ to −20‰ in the uppermost 3 mm and oscillated repeatedly between −10‰ and −30‰ down to a depth of 8 mm. These variations are attributed to spatially variable bacterial sulfate reduction within the mat. A parallel examination of the spatial distribution of known sulfate-reducing bacteria within the family Desulfobacteraceae was conducted using catalyzed reporter deposition fluorescence in situ hybridization. Significant concentrations of Desulfobacteraceae were observed in both oxic and anoxic zones of the mat and occurred in several distinct layers, in large aggregates and heterogeneously dispersed as single cells throughout. The spatial distribution of these microorganisms is consistent with the variation in sulfide concentration and isotopic composition we observed. The parallel application of the methodologies developed here can shed light on micron-scale sulfur cycling within microbially dominated sedimentary environments.
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Anbar AD, Knoll AH . (2002). Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297: 1137–1142.
Baumgartner LK, Reid RP, Dupraz C, Decho AW, Buckley DH, Spear JR et al. (2006). Sulfate reducing bacteria in microbial mats: changing paradigms, new discoveries. Sediment Geol 185: 131–145.
Brunner B, Bernasconi SM . (2005). A revised isotope fractionation model for dissimilatory sulfate reduction in sulfate reducing bacteria. Geochimica et Cosmochimica Acta 69: 4759–4771.
Canfield DE . (2001). Biogeochemistry of sulfur isotopes. Rev Mineral Geochem 43: 607–636.
Canfield DE, Des Marais DJ . (1993). Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochimica Et Cosmochimica Acta 57: 3971–3984.
Canfield DE, Teske A . (1996). Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 382: 127–132.
Cline JD . (1969). Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14: 454–458.
Clode PL, Stern RA, Marshall AT . (2007). Subcellular imaging of isotopically labeled carbon compounds in a biological sample by ion microprobe (NanoSIMS). Microsc Res Tech 70: 220–229.
Cypionka H . (2000). Oxygen respiration by Desulfovibrio species. Annu Rev Microbiol 54: 827–848.
Decho AW, Visscher PT, Reid RP . (2005). Changes in microspatial organization of bacteria during development of surface microbial mats of marine lithifying stromatolites determined using combined FISH/GIS-image analyses. Geophys Res Abstr 7: 07807.
Decker KLM, Potter CS, Bebout BM, Des Marais DJ, Carpenter S, Discipulo M et al. (2005). Mathematical simulation of the diel O, S, and C biogeochemistry of a hypersaline microbial mat. Fems Microbiol Ecol 52: 377–395.
Des Marais DJ, Cohen Y, Nguyen H, Cheatham M, Cheatham T, Munos E . (1989). Carbon isotopic trends in the hypersaline ponds and microbial mats at Guerrero Negro, Baja California Sur, Mexico: implications for precambrian stromatolites. In: Cohen Y, Rosenberg E. (eds). Microbial Mats: Physiological Ecology of Benthic Microbial Communities. American Society for Microbiology: Washington, DC, pp 191–203.
Dupraz C, Visscher PT, Baumgartner LK, Reid RP . (2004). Microbe-mineral interactions: early carbonate precipitation in a hypersaline lake (Eleuthera Island, Bahamas). Sedimentology 51: 745–765.
Fike DA, Grotzinger JP, Pratt LM, Summons RE . (2006). Oxidation of the Ediacaran ocean. Nature 444: 744–747.
Frund C, Cohen Y . (1992). Diurnal cycles of sulfate reduction under oxic conditions in cyanobacterial mats. Appl Environ Microbiol 58: 70–77.
Gill BC, Lyons TW, Saltzman MR . (2007). Parallel, high-resolution carbon and sulfur isotope records of the evolving Paleozoic marine sulfur reservoir. Palaeogeogr Palaeoclimatol Palaeoecol 256: 156–173.
Grotzinger JP, Knoll AH . (1999). Stromatolites in precambrian carbonates: evolutionary mileposts or environmental dipsticks? Annu Rev Earth Planet Sci 27: 313–358.
Habicht KS, Canfield DE . (1996). Sulphur isotope fractionation in modern microbial mats and the evolution of the sulphur cycle. Nature 382: 342–343.
Habicht KS, Canfield DE, Rethmeier J . (1998). Sulfur isotope fractionation during bacterial reduction and disproportionation of thiosulfate and sulfite. Geochimica Et Cosmochimica Acta 62: 2585–2595.
Habicht KS, Gade M, Thamdrup B, Berg P, Canfield DE . (2002). Calibration of sulfate levels in the Archean ocean. Science 298: 2372–2374.
Hayes JM, Waldbauer JR . (2006). The carbon cycle and associated redox processes through time. Philos Trans R Soc Lond B Biol Sci 361: 931–950.
Hoehler TM, Bebout BM, Des Marais DJ . (2001). The role of microbial mats in the production of reduced gases on the early Earth. Nature 412: 324–327.
Hoppe P, Mostefaoui S, Stephan T . (2005). O- and S-isotope imaging of primitive solar system materials with the Mainz NanoSIMS. Geochimica Et Cosmochimica Acta 69: A523.
Hurtgen MT, Arthur MA, Halverson GP . (2005). Neoproterozoic sulfur isotopes, the evolution of microbial sulfur species, and the burial efficiency of sulfide as sedimentary pyrite. Geology 33: 41–44.
Jeroschewsky P, Steuckart C, Kuehl M . (1996). An amperometric microsensor for the determination of H2S in aquatic environments. Anal Chem 68: 4351–4357.
Jorgensen BB . (1994). Sulfate reduction and thiosulfate transformations in a cyanobacterial mat during a diel oxygen cycle. FEMS Microbiol Ecol 13: 303–312.
Jorgensen BB, Revsbech NP, Blackburn TH, Cohen Y . (1979). Diurnal cycle of oxygen and sulfide microgradients and microbial photosynthesis in a cyanobacterial mat sediment. Appl Environ Microbiol 38: 46–58.
Kampschulte A, Strauss H . (2004). The sulfur isotopic evolution of Phanerozoic seawater based on the analysis of structurally substituted sulfate in carbonates. Chem Geol 204: 255–286.
Krekeler D, Sigalevich P, Teske A, Cypionka H, Cohen Y . (1997). A sulfate-reducing bacterium from the oxic layer of a microbial mat from Solar Lake (Sinai), Desulfovibriooxyclinae sp. nov. Arch Microbiol 167: 369–375.
Kuehl M, Steuckart C, Eickert G, Jeroschewsky P . (1998). A H2S microsensor for profiling biofilms and sediments: application in an acidic lake sediment. Aquat Microb Ecol 15: 201–209.
Ley RE, Harris JK, Wilcox J, Spear JR, Miller SR, Bebout BM et al. (2006). Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl Environ Microbiol 72: 3685–3695.
Li T, Wu TD, Mazeas L, Toffin L, Guerquin-Kern JL, Leblon G et al. (2008). Simultaneous analysis of microbial identity and function using NanoSIMS. Environ Microbiol 10: 580–588.
Loy A, Maixner F, Wagner M, Horn M . (2007). ProbeBase—an online resource for rRNA-targeted oligonucleotide probes: new features 2007. Nucleic Acids Res 35: D800–D804.
Manz W, Eisernbrecher M, Neu TR, Szewzyk U . (1998). 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: 43–61.
Minz D, Fishbain S, Green SJ, Muyzer G, Cohen Y, Rittmann BE et al. (1999a). 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: 4659–4665.
Minz D, Flax JL, Green SJ, Muyzer G, Cohen Y, Wagner M et al. (1999b). Diversity of sulfate-reducing bacteria in oxic, anoxic regions of a microbial mat characterized by comparative analysis of dissimilatory sulfite reductase genes. Appl Environ Microbiol 65: 4666–4671.
Musselwhite CL, Swift D, Gilpen J, McInerney MJ . (2007). Spatial variability of sulfate reduction in a shallow aquifer. Environ Microbiol 9: 2810–2819.
Pernthaler A, Pernthaler J, Amann R . (2002). Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68: 3094–3101.
Pernthaler A, Pernthaler J, Amann R . (2004). Molecular Microbial Ecology Manual. Kluwer Academic Press: Dordrecht, The Netherlands.
Porter D, Roychoudhury AN, Cowan D . (2007). Dissimilatory sulfate reduction in hypersaline coasal pans: activity across a salinity gradient. Geochimica Et Cosmochimica Acta 71: 5102–5116.
Revsbech NP . (1989). An oxygen sensor with a guard cathode. Limnol Oceanogr 34: 474–478.
Revsbech NP, Jorgensen BB, Blackburn TH, Cohen Y . (1983). Microelectrode studies of the photosynthesis and O2, H2S, and pH profiles of a microbial mat. Limnol Oceanogr 28: 1062–1074.
Risatti JB, Capman WC, Stahl DA . (1994). Community structure of a microbial mat: the phylogenetic dimension. Proc Natl Acad Sci USA 91: 10173–10177.
Sigalevich P, Baev MV, Teske A, Cohen Y . (2000). 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: 5005–5012.
Slodzian G, Hillion F, Stadermann FJ, Zinner E . (2004). QSA influences on isotopic ratio measurements. Appl Surf Sci 231–2: 874–877.
Sorensen KB, Canfield DE, Teske AP, Oren A . (2005). Community composition of a hypersaline endoevaporitic microbial mat. Appl Environ Microbiol 71: 7352–7365.
Spear JR, Ley RE, Berger AB, Pace NR . (2003). Complexity in natural microbial ecosystems: the Guerrero Negro experience. Biol Bull 204: 168–173.
Steedman HF . (1957). Polyester wax: a new ribboning embedding medium for histology. Nature 179: 1345.
Studley SA, Ripley EM, Elswick ER, Dorais MJ, Fong J, Finkelstein D et al. (2002). Analysis of sulfides in whole rock matrices by elemental analyzer-continuous flow isotope ratio mass spectrometry. Chem Geol 192: 141–148.
Teske A, Ramsing NB, Habicht K, Fukui M, Kuver J, Jorgensen BB et al. (1998). Sulfate-reducing bacteria and their activities in cyanobacterial mats of Solar Lake (Sinai, Egypt). Appl Environ Microbiol 64: 2943–2951.
Tonolla M, Peduzzi R, Hahn D . (2005). Long-term population dynamics of phototrophic sulfur bacteria in the chemocline of Lake Cadagno, Switzerland. Appl Environ Microbiol 71: 3544–3550.
Visscher PT, Baumgartner LK, Buckley DH, Rogers DR, Hogan ME, Raleigh CD et al. (2003). Dimethyl sulphide and methanethiol formation in microbial mats: potential pathways for biogenic signatures. Environ Microbiol 5: 296–308.
Visscher PT, Reid RP, Bebout BM . (2000). Microscale observations of sulfate reduction: Correlation of microbial activity with lithified micritic laminae in modern marine stromatolites. Geology 28: 919–922.
Wieland A, de Beer D, Damgaard LR, Kuehl M, van Dusschoten D, Van As H . (2001). Fine-scale measurement of diffusivity in a microbial mat with nuclear magnetic resonance imaging. Limnol Oceanogr 46: 248–259.
Wieland A, Kuehl M, McGowan L, Sole A, Diestra E, Esteve I et al. (2003). Microbial mats on the Orkney Islands revisited: microenvironment and microbial community composition. Microb Ecol 46: 371–390.
Wieland A, Zopfi J, Benthien A, Kuhl M . (2005). Biogeochemistry of an iron-rich hypersaline microbial mat (Camargue, France). Microb Ecol 49: 34–49.
Wieringa EBA, Overmann J, Cypionka H . (2000). Detection of abundant sulphate-reducing bacteria in marine oxic sediment layers by a combined cultivation and molecular approach. Environ Microbiol 2: 417–427.
Wortmann UG, Bernasconi SM, Boettcher ME . (2001). Hypersulfidic deep biosphere indicates extreme sulfur isotope fractionation during single step microbial sulfate reduction. Geology 29: 647–650.
Acknowledgements
We would like to acknowledge the Gordon and Betty Moore Foundation and the Caltech Center for Geochemical and Cosmochemical Microanalysis for funding (to VJO) as well as support from National Aeronautics and Space Administration Grant NAI02-003-0001 issued through the Astrobiology Program. DAF was supported by the Caltech OK Earl Postdoctoral Fellowship. CLG was supported by a National Science Foundation Graduate Research Fellowship. We would like to thank Yunbin Guan, John Eiler and Tina Treude for analytical assistance and invaluable discussions, Bill Ussler for discussions and assistance with methodological development, Frank Stadermann for discussions and Dirk de Beer for a critical reading of this manuscript. We are also indebted to the NASA Ames group (Tori Hoehler, Niko Finke, Kendra Turk, Mike Kubo, Linda Jahnke and David DesMarais) for support and assistance with sample collections.
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Fike, D., Gammon, C., Ziebis, W. et al. Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-FISH approach. ISME J 2, 749–759 (2008). https://doi.org/10.1038/ismej.2008.39
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DOI: https://doi.org/10.1038/ismej.2008.39


