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Molecular Analysis of the Spatio-temporal Distribution of Sulfate-reducing Bacteria (SRB) in Camargue (France) Hypersaline Microbial Mat

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Abstract

The spatio-temporal distribution of sulfate-reducing bacteria (SRB) in the microbial mat of Camargue (Salins-de-Giraud, France) was investigated by molecular approaches at both microscale spatial resolution and different taxonomic organization levels. The vertical distribution of the SRB populations was correlated with oxygen and sulfide microgradient fluctuations. Comparisons of Terminal restriction fragment length polymorphism (T-RFLP) fingerprints showed distinct locations of some operational taxonomic units at daytime and at night (4:00 or 15:00 hours) revealing important differences on the structures of the bacterial communities. When oxygen penetrates the mat, SRB migration was observed either downward to reach deeper anoxic zones to escape oxygen or upward to reach oxic surface zones. When no migration was observed, both metabolism switches and aggregate formations were suspected. These behaviors allowed the aerotolerant SRB to deal with oxygen. The analysis of the DesulfococcusDesulfonemaDesulfosarcina T-RFLP profiles revealed up-migrating populations related to both Desulfonema sp. and Desulfosarcina variabilis. T-RFLP profiles combined with 16S ribosomal ribonucleic acid gene library analysis of the Desulfobacter group revealed two distinct populations: a population related to the recently described Desulfotignum genus migrating upward during the night and a population of a new species of the Desulfobacter uniformly located throughout the mat independent of the period. Thus, the identification of the new oxygen-tolerant SRB will provide the basis for understanding the physiological adaptations to oxygen.

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References

  1. Baumgartner LK, Reid RP, Dupraz C, Decho AW, Buckley DH, Spear JR, Przekop KM, Visscher, PT (2006) Sulfate reducing bacteria in microbial mats: changing paradigms, new discoveries. Sediment Geol 185:131–145

    Article  CAS  Google Scholar 

  2. Canfield DE, Des Marais DJ (1991) Aerobic sulfate reduction in microbial mats. Science 251:1471–1473

    Article  PubMed  CAS  Google Scholar 

  3. Caumette P, Matheron R, Raymond N, Relexans JC (1994) Microbial mats in the hypersaline ponds of Mediterranean salterns (Salins-de-Giraud, France). FEMS Microbiol Ecol 13:273–286

    Article  CAS  Google Scholar 

  4. Cohen Y (1984) Oxygenic photosynthesis, anoxygenic photosynthesis, and sulfate reduction in cyanobacterial mats. In: Klug MJ, Ready CA (eds) Current perspectives in microbial ecology. American Society for Microbiology, Washington, DC, pp 435–441

    Google Scholar 

  5. Cypionka H, Widdel F, Pfennig N (1985) Survival of sulfate-reducing bacteria after oxygen stress, and growth in sulfate-free oxygen-sulfide gradients. FEMS Microbiol Lett 31:39–45

    Article  CAS  Google Scholar 

  6. Daly K, Sharp RJ, McCarthy AJ (2000) Development of oligonucleotide probes and PCR primers for detecting phylogenetic subgroups of sulfate-reducing bacteria. Microbiology 146:1693–1705

    PubMed  CAS  Google Scholar 

  7. Dannenberg S, Kroder M, Dilling W, Cypionka H (1992) Oxidation of H2, organic compounds and inorganic sulfur compounds coupled to reduction of O2 or nitrate by sulfate reducing-bacteria. Arch Microbiol 158:93–99

    Article  CAS  Google Scholar 

  8. Dilling W, Cypionka H (1990) Aerobic respiration in sulfate-reducing bacteria. FEMS Microbiol Lett 71:123–128

    CAS  Google Scholar 

  9. Dolla A, Fournier M, Dermoun Z (2006) Oxygen defense in sulfate-reducing bacteria. J Biotechnol 126:87–100

    Article  PubMed  CAS  Google Scholar 

  10. Dolla A, Fu R, Brumlik MJ, Voordouw G (1992) Nucleotide sequence of dcrA, a Desulfovibrio vulgaris Hildenborough chemoreceptor gene and its expression in Escherichia coli. J Bacteriol 174:1726–1733

    PubMed  CAS  Google Scholar 

  11. Eschemann A, Kühl M, Cypionka H (1999) Aerotaxis in Desulfovibrio. Environ Microbiol 1:489–494

    Article  PubMed  CAS  Google Scholar 

  12. Ferris MJ, Ward DM (1997) Seasonal distributions of dominant 16S rRNA-defined populations in a hot spring microbial mat examined by denaturing gradient gel electrophoresis. Appl Environ Microbiol 63:1375–1381

    PubMed  CAS  Google Scholar 

  13. Foti M, Sorokin DY, Lomans B, Mussman M, Zacharova EE, Pimenov NV, Kuenen JG, Muyzer G (2007) Diversity, activity, and abundance of sulfate-reducing bacteria in saline and hypersaline soda lakes. Appl Environ Microbiol 73:2093–2100

    Article  PubMed  CAS  Google Scholar 

  14. Fourçans A, García de Oteyza T, Wieland A, Solé A, Diestra E, van Bleijswijk J, Grimalt JO, Kühl M, Esteve I, Muyzer G, Caumette P, Duran R (2004) Characterization of functional bacterial groups in a hypersaline microbial mat community (Salins-de-Giraud, Camargue, France). FEMS Microbiol Ecol 51:55–70

    Article  PubMed  CAS  Google Scholar 

  15. Fourçans A, Solé A, Diestra E, Ranchou-Peyruse A, Esteve I, Caumette P, Duran R (2006) Vertical migration of phototrophic bacterial populations in a hypersaline microbial mat from Salins-de-Giraud (Camargue, France). FEMS Microbiol Ecol 57:367–377

    Article  PubMed  CAS  Google Scholar 

  16. Fournier M, Zhang Y, Wildschut JD, Dolla A, Voordouw JK, Schriemer DC, Voordouw G (2003) Function of oxygen resistance proteins in the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. J Bacteriol 185:71–79

    Article  PubMed  CAS  Google Scholar 

  17. Fründ C, Cohen Y (1992) Diurnal cycles of sulfate reduction under oxic conditions in cyanobacterial mats. Appl Environ Microbiol 58:70–77

    PubMed  Google Scholar 

  18. Fukui M, Teske A, Aßmus B, Muyzer G, Widdel F (1999) Physiology, phylogenetic relationships, and ecology of filamentous sulfate-reducing bacteria (genus Desulfonema). Arch Microbiol 172:193–203

    Article  PubMed  CAS  Google Scholar 

  19. Giani D, Seeler J, Giani L, Krumbein WE (1989) Microbial mats and physicochemistry in a saltern in the Bretagne (France) and in a laboratory scale saltern model. FEMS Microbiol Ecol 62:151–162

    Article  CAS  Google Scholar 

  20. Jonkers HM, Koh IO, Behrend P, Muyzer G, de Beer D (2005) Aerobic organic carbon mineralization by sulfate-reducing bacteria in the oxygen-saturated photic zone of a hypersaline microbial mat. Microb Ecol 49:291–300

    Article  PubMed  CAS  Google Scholar 

  21. Jørgensen BB (1994) Sulfate reduction and thiosulfate transformations in a cyanobacterial mat during a diel oxygen cycle. FEMS Microbiol Ecol 13:303–312

    Google Scholar 

  22. Kovach WL (1999) MVSP - a Multivariate Statistical Package for Windows. ver. 3.1. ed. Kovack Computing Services, Wales, UK

    Google Scholar 

  23. Krekeler D, Sigalevich P, Teske A, Cohen Y, Cypionka H (1997) A sulfate-reducing bacterium from the oxic layer of a microbial mat from Solar Lake (Sinai), Desulfovibrio oxyclinae sp. nov. Arch Microbiol 167:369–375

    Article  CAS  Google Scholar 

  24. Krekeler D, Teske A, Cypionka H (1998) Strategies of sulfate-reducing bacteria to escape oxygen stress in a cyanobacterial mat. FEMS Microbiol Ecol 25:89–96

    Article  CAS  Google Scholar 

  25. Kuever J, Konneke M, Galushko A, Drzyzga O (2001) Reclassification of Desulfobacterium phenolicum as Desulfobacula phenolica comb. nov. and description of strain SaxT as Desulfotignum balticum gen. nov., sp. nov. Int J Syst Evol Microbiol 51:171–177

    PubMed  CAS  Google Scholar 

  26. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245

    Article  PubMed  CAS  Google Scholar 

  27. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stachenbradt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175

    Google Scholar 

  28. Liu WT, Marsh TL, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63:4516–4522

    PubMed  CAS  Google Scholar 

  29. Maidak BL, Cole JR, Lilburn TG, Parker CT Jr., Saxman PR, Farris RJ, Garrity GM, Olsen GJ, Schmidt TM, Tiedje JM (2001) The RDP-II (Ribosomal Database Project). Nucl Acids Res 29:173–174

    Article  PubMed  CAS  Google Scholar 

  30. Marschall C, Frenzel C, Cypionka H (1993) Influence of oxygen on sulphate reduction and growth of sulphate-reducing bacteria. Arch Microbiol 159:168–173

    Article  CAS  Google Scholar 

  31. Minz D, Fishbain S, Green SJ, Muyzer G, Cohen Y, Rittmann BE, Stahl DA (1999) 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

    PubMed  CAS  Google Scholar 

  32. Minz D, Flax JL, Green SJ, Muyzer G, Cohen Y, Wagner M, Rittmann BE, Stahl DA (1999) 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 65:4666–4671

    PubMed  CAS  Google Scholar 

  33. Mouné S, Caumette P, Matheron R, Willison JC (2003) Molecular sequence analysis of prokaryotic diversity in the anoxic sediments underlying cyanobacterial mats of two hypersaline ponds in Mediterranean salterns. FEMS Microbiol Ecol 44:117–130

    Article  CAS  PubMed  Google Scholar 

  34. Namsaraev ZB, Gorlenko VM, Namsaraev BB, Buriukhaev SP, Iurkov VV (2003) The structure and biogeochemical activity of the phototrophic communities from the Bol’sherechenskii alkaline hot spring. Mikrobiologiia 72:228–238

    PubMed  CAS  Google Scholar 

  35. Ramsing NB, Ferris MJ, Ward DM (2000) Highly ordered vertical structure of Synechococcus populations within the one-millimeter-thick photic zone of a hot spring cyanobacterial mat. Appl Environ Microbiol 66:1038–1049

    Article  PubMed  CAS  Google Scholar 

  36. Ramsing NB, Kühl M, Jørgensen BB (1993) Distribution of sulfate-reducing bacteria, O2, and H2S in photosynthetic biofilms determined by oligonucleotide probes and microelectrodes. Appl Environ Microbiol 59:3840–3849

    PubMed  CAS  Google Scholar 

  37. 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

    Article  Google Scholar 

  38. Risatti JB, Capman WC, Stahl DA (1994) Community structure of a microbial mat: the phylogenetic dimension. Proc Natl Acad Sci USA 91:10173–10177

    Article  PubMed  CAS  Google Scholar 

  39. Ruff-Roberts AL, Kuenen JG, Ward DM (1994) Distribution of cultivated and uncultivated cyanobacteria and Chloroflexus-like bacteria in hot spring microbial mats. Appl Environ Microbiol 60:697–704

    PubMed  CAS  Google Scholar 

  40. Saitou N, Nei M (1987) The Neighbor-joining Method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  41. Sass AM, Eschemann A, Kühl M, Tharb R, Sass H, Cypionka H (2002) Growth and chemosensory behavior of sulfate-reducing bacteria in oxygen–sulfide gradients. FEMS Microbiol Ecol 40:47–54

    CAS  PubMed  Google Scholar 

  42. Schink B, Thiemann V, Laue H, Friedrich MW (2002) Desulfotignum phosphitoxidans sp. nov., a new marine sulfate reducer that oxidizes phosphite to phosphate. Arch Microbiol 177:381–391

    Article  PubMed  CAS  Google Scholar 

  43. Sigalevich P, Meshorer E, Helman Y, Cohen Y (2000) Transition from anaerobic to aerobic growth conditions for the sulfate- reducing bacterium Desulfovibrio oxyclinae results in flocculation. Appl Environ Microbiol 66:5005–5012

    Article  PubMed  CAS  Google Scholar 

  44. Sorokin DI, Turova TP, Kuznetsov BB, Briantseva IA, Gorlenko VM (2000) Roseinatronobacter thiooxidans gen. nov., sp. nov., a new alkaliphilic aerobic bacteriochlorophyll-alpha-containing bacteria from a soda lake. Mikrobiologiia 69:89–97

    PubMed  Google Scholar 

  45. Teske A, Ramsing NB, Habicht K, Fukui M, Kuver J, Jørgensen BB, Cohen Y (1998) Sulfate-reducing bacteria and their activities in cyanobacterial mats of solar lake (Sinai, Egypt). Appl Environ Microbiol 64:2943–2951

    PubMed  CAS  Google Scholar 

  46. Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  47. Weisburg, WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed  CAS  Google Scholar 

  48. Whale GF, Walsby AE (1984) Motility of the cyanobacterium Microcoleus chthonoplastes in mud. Phycol J 19:117–123

    Article  Google Scholar 

  49. Wieland A, Kuhl M (2006) Regulation of photosynthesis and oxygen consumption in a hypersaline cyanobacterial mat (Camargue, France) by irradiance, temperature and salinity. FEMS Microbiol Ecol 55:195–210

    Article  PubMed  CAS  Google Scholar 

  50. Wieland A, Kuhl M, McGowan L, Fourçans A, Duran R, Caumette P, Garcia De Oteyza T, Grimalt JO, Solé A, Diestra E, Esteve I, Herbert RA (2003) Microbial mats on the Orkney islands revisited: microenvironment and microbial community composition. Microb Ecol 46:371–390

    Article  PubMed  CAS  Google Scholar 

  51. Wieland A, Zopfi J, Benthien M, Kühl M (2005) Biogeochemistry of an iron-rich hypersaline microbial mat (Camargue, France). Microb Ecol 49:34–49

    Article  PubMed  CAS  Google Scholar 

  52. Wieringa EB, 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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We acknowledge the financial support provided by the EC (MATBIOPOL project, grant EVK3-CT-1999-00010) and by the “Conseil Régional d’Aquitaine.” The authors are grateful to the Company of Salins-du-midi at Salins-de-Giraud for facilitating access to the salterns, sampling, and field experiments. AF is partly supported by a doctoral grant from the general council of Atlantic Pyrenees. Dr. Remignon (ENSAT, Toulouse, France) is gratefully thanked for the technical support. Thanks also to anonymous reviewers for their helpful comments and suggestions. The authors are especially indebted to Prof. Jim Spain and C. Mroz for careful reading of the English and for helpful comments on the paper.

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Fourçans, A., Ranchou-Peyruse, A., Caumette, P. et al. Molecular Analysis of the Spatio-temporal Distribution of Sulfate-reducing Bacteria (SRB) in Camargue (France) Hypersaline Microbial Mat. Microb Ecol 56, 90–100 (2008). https://doi.org/10.1007/s00248-007-9327-x

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  • DOI: https://doi.org/10.1007/s00248-007-9327-x

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