Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): Abundance and diversity related to geochemical zonation

Environmental Microbiology

Volumn 11, Issue 5, 2009, Pages 1278-1291

  Leloup, Julie ^a   Fossing, Henrik ^b   Kohls, Katharina ^c   Holmkvist, Lars ^c   Borowski, Christian ^c   Jørgensen, Bo Barker ^c,d  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b Department of Inland Fisheries   (Denmark)

^c MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; RIBOSOME DNA; RNA 16S; SULFATE;

ARTICLE; BACTERIAL COUNT; BACTERIAL GENE; BACTERIUM; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DENMARK; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHYLOGENY; SEDIMENT;

BACTERIA; BIODIVERSITY; CLUSTER ANALYSIS; COLONY COUNT, MICROBIAL; DENMARK; DNA, BACTERIAL; DNA, RIBOSOMAL; GENES, BACTERIAL; GEOLOGIC SEDIMENTS; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SULFATES;

BACTERIA (MICROORGANISMS); DESULFOBACTERACEAE; DESULFOBACTERIUM; DESULFOCOCCUS; DESULFOSARCINA; POSIBACTERIA;

EID: 65349096123     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2008.01855.x     Document Type: Article

References (62)

1. Bahr, M., Crump, B.C., Klepac-Ceraj, V., Teske, A., Sogin, M.L. Hobbie, J.E. (2005) Molecular characterization of sulfate-reducing bacteria in a New England salt marsh. Environ Microbiol 7 : 1175 1185. (Pubitemid 41026517)
2. Barton, L.L. Tomei, F.A. (1995) Characteristics and activities of sulfate-reducing bacteria. In Sulfate-reducing Bacteria. Barton, L.L. (ed.). New York, NY, USA : Peplum Press, pp. 1 32.
3. Canfield, D.E. (1989) Sulfate reduction and oxic respiration in marine sediments: implications for organic carbon preservation in euxinic environments. Deep Sea Res 36 : 121 138. (Pubitemid 19306183)
4. Castro, H., Reddy, K.R. Ogram, A. (2002) Composition and function of sulfate-reducing prokaryotes in eutrophic and pristine areas of the Florida Everglades. Appl Environ Microbiol 68 : 6129 6137. (Pubitemid 36342449)
5. Dale, A.W., Aguilera, D.R., Regnier, P., Fossing, H., Knab, N.J. Jørgensen, B.B. (2008) Seasonal dynamics of the depth and rate of anaerobic oxidation of methane in Aarhus Bay (Denmark). J Mar Res 6 : 127 155.
6. Dell'Anno, A., Fabiano, M., Mei, M.L. Danovaro, R. (1998) Nucleic acid (DNA, RNA) quantification and RNA/DNA ratio determination in marine sediments: comparison of spectrophotometric, fluorometric, and high-performance liquid chromatography methods and estimation of detrital DNA. Appl Environ Microbiol 64 : 3238 3245. (Pubitemid 28411442)
7. Demanèche, S., Jocteur-Monrozier, L., Quincampoix, H. Simonet, P. (2001) Evaluation of biological and physical protection against nuclease degradation of clay-bound plasmid DNA. Appl Environ Microbiol 67 : 293 299. (Pubitemid 32044431)
8. Devereux, R., Delaney, M., Widdel, F. Stahl, D.A. (1989) Natural relationships among sulfate-reducing Eubacteria. J Bacteriol 171 : 6689 6695. (Pubitemid 20006952)
9. Dhillon, A., Teske, A., Dillon, J., Stahl, D.A. Sogin, M.L. (2003) Molecular characterization of sulfate-reducing bacteria in the Guaymas basin. Appl Environ Microbiol 69 : 2765 2772. (Pubitemid 36560355)
10. Felsenstein, J. (1995) PHYLIP: Phylogeny Inference Package. Seattle, WA, USA : Department of Genetics, University of Washington.
11. Fossing, H. Jørgensen, B.B. (1989) Measurements of bacterial sulfate reduction in sediments: evaluation of a single step chromium reduction method. Biogeochemistry 8 : 205 222. (Pubitemid 20401699)
12. Fossing, H., Ferdelman, T.G. Berg, P. (2000) Sulfate reduction and methane oxidation in continental margin sediments influenced by irrigation (South-East Atlantic off Namibia). Geochim Cosmochim Acta 64 : 897 910. (Pubitemid 30218448)
13. Foti, M., Sorokin, D.Y., Lomans, B., Mussman, M., Zacharova, E.E., Pimenov, N.V., et al. (2007) Diversity, activity and abundance of sulfate-reducing bacteria in saline and hypersaline soda Lakes. Appl Environ Microbiol 73 : 2093 2100. (Pubitemid 46649498)
14. Geets, J., Borremans, B., Diels, L., Springael, D., Vangronsveld, J., van der Lelie, D. Vanbroekhoven, K. (2006) DsrB gene-based DGGE for community and diversity surveys of sulfate-reducing bacteria. J Microbiol Methods 66 : 194 205. (Pubitemid 43922387)
15. Guyot, J.P. Brauman, A. (1986) Methane production from formate by synthrophic association of Methanobacterium bryantii and Desulfovibrio vulgaris JJ. Appl Environ Microbiol 52 : 1436 1437. (Pubitemid 17203879)
16. Hines, M.E., Evans, R.S., Sharak Genthner, B.R., Willis, S.G., Friedman, S., Rooney-Varga, J.N. Devereux, R. (1999) Molecular phylogenetic and biogeochemical studies of sulfate-reducing bacteria in the rhizosphere of Spartina alterniflora. Appl Environ Microbiol 65 : 2209 2216. (Pubitemid 129526222)
17. Holmes, D.E., Bond, D.R. Lovley, D.R. (2004) Electron transfer by Desulfobulbus propionicus to Fe(III) and graphite electrodes. Appl Environ Microbiol 70 : 1234 1237. (Pubitemid 38568255)
18. Hurlbert, S.H. (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52 : 577 586.
19. Isaksen, M.F., Bak, F. Jørgensen, B.B. (1994) Thermophilic sulfate-reducing bacteria in cold marine sediment. FEMS Microbiol Ecol 14 : 1 8. (Pubitemid 24122432)
20. Jørgensen, B.B. (1978) A comparison of methods for the quantification of bacterial sulfate reduction in coastal marine sediments. I. Measurement with radiotracer techniques. Geomicrobiol J 1 : 11 27.
21. Jørgensen, B.B. (1982) Mineralization of organic matter in the sea bed - the role of sulphate reduction. Nature 296 : 643 645. (Pubitemid 12263228)
22. Jørgensen, B.B. (1996) Case study - Aarhus Bay, eutrophication in coastal marine ecosystems. Am Geophys Union 52 : 137 154.
23. Jørgensen, B.B. Bak, F. (1991) Pathways and microbiology of thiosulfate reduction in a marine sediment (Kattegat, Denmark). Appl Environ Microbiol 57 : 847 856.
24. Jørgensen, B.B. Fenchel, T. (1974) The sulfur cycle of a marine model system. Mar Biol 24 : 189 201.
25. Karr, E.A., Sattley, W.M., Rice, M.R., Jung, D.O., Madigan, M.T. Achenbach, L.A. (2005) Diversity and distribution of sulfate-reducing bacteria in permanently frozen lake Fryxell, McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 71 : 6353 6359. (Pubitemid 41456936)
26. Klappenbach, J.L., Saxman, P.H., Cole, J.R. Schmidt, T.M. (2001) rrndb: the ribosomal RNA operon copy number database. Nucleic Acids Res 29 : 181 184. (Pubitemid 32054441)
27. Klein, M., Friedrich, M., Roger, A.J., Hugenholtz, P., Fishbain, S., Abicht, H., et al. (2001) Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. Appl Environ Microbiol 67 : 6028 6035. (Pubitemid 32917422)
28. Knoblauch, C., Jørgensen, B.B. Harder, J. (1999) Community size and metabolic rates of psychrophilic sulfate-reducing bacteria in Arctic marine sediments. Appl Environ Microbiol 65 : 4230 4233. (Pubitemid 129519891)
29. Kondo, R., Nedwell, D.B., Purdy, K.J. de Queiroz Silva, S. (2004) Detection and enumeration of sulphate-reducing bacteria in estuarine sediments. Geomicrobiol J 21 : 145 157. (Pubitemid 38462161)
30. Lehours, A.-C., Bardot, C., Thenot, A., Debroas, D. Fonty, G. (2005) Anaerobic microbial communities in Lake Pavin, a unique meromictic lake in France. Appl Environ Microbiol 71 : 7389 7400. (Pubitemid 43194233)
31. Leloup, J., Quillet, L., Oger, C., Boust, D. Petit, F. (2004) Molecular quantification of sulfate-reducing microorganisms (carrying dsrAB genes) by competitive PCR in estuarine sediments. FEMS Microbiol Ecol 47 : 207 214. (Pubitemid 38177583)
32. Leloup, J., Quillet, L., Berthe, T. Petit, F. (2006) Diversity of the dsrAB (dissimilatory sulfite reductase) gene sequences from two contrasting mudflats of the Seine estuary, France. FEMS Microbiol Ecol 55 : 230 238.
33. Leloup, J., Loy, A., Knab, N.J., Borowski, C., Wagner, M. Jørgensen, B.B. (2007) Diversity and abundance of sulfate-reducing microorganisms in the sulfate and methane zones of a marine sediment, Black Sea. Environ Microbiol 9 : 131 142. (Pubitemid 46061397)
34. Liu, X., Bagwell, C.E., Wu, L., Devol, A.H. Zhou, J. (2003) Molecular diversity of sulfate-reducing bacteria from two different continental margin habitats. Appl Environ Microbiol 69 : 6073 6081. (Pubitemid 37280331)
35. Luna, G.M., Manini, E. Danovaro, R. (2002) Large fraction of dead and inactive bacteria in coastal marine sediments: comparison of protocols for determination and ecological significance. Appl Environ Microbiol 68 : 3509 3513. (Pubitemid 34734052)
36. Manini, E. Danovaro, R. (2006) Synoptic determination of living/dead and active/dormant bacterial fractions in marine sediments. FEMS Microbiol Ecol 55 : 416 423.
37. Mills, H.J., Martinez, R.J., Story, S. Sobecky, P.A. (2005) Characterization of microbial community structure in Gulf of Mexico gas hydrates: comparative analysis of DNA- and RNA-derived clone libraries. Appl Environ Microbiol 71 : 3235 3247. (Pubitemid 40807235)
38. Mußmann, M., Ishii, K., Rabus, R. Amann, R. (2005a) Diversity and vertical distribution of cultured and uncultured Deltaproteobacteria in an intertidal mudflat of the Wadden Sea. Environ Microbiol 7 : 405 418. (Pubitemid 40290129)
39. Mußmann, M., Richter, M., Lombardot, T., Meyerdierks, A., Kuever, J., Kube, M., et al. (2005b) Clustered genes related to sulfate respiration in uncultured prokaryotes support the theory of their concomitant horizontal transfer. J Bacteriol 187 : 7126 7137. (Pubitemid 41428889)
40. Muyzer, G. Stams, A.J.M. (2008) The ecology and biotechnology of sulfate-reducing bacteria. Nat Rev Microbiol 6 : 441 545.
41. Muyzer, G., De Waal, E.C. Uitterlinden, A. (1993) Profiling of complex microbial populations by denaturating gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59 : 695 700. (Pubitemid 23072343)
42. Nadkarni, M.A., Martin, F.E., Jacques, N.A. Hunter, N. (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148 : 257 266. (Pubitemid 34083204)
43. Nercessian, O., Bienvenu, N., Moreira, D., Prieur, D. Jeanthon, C. (2005) Diversity of functional genes of methanogens, methanotrophs and sulfate-reducers in deep-sea hydrothermal environments. Environ Microbiol 7 : 118 132.
44. Nocker, A. Camper, A.K. (2006) Selective removal of DNA from dead cells of mixed bacterial communities by use of Ethidium Monoazide. Appl Environ Microbiol 72 : 1997 2004.
45. Pérez-Jiménez, J.R. Kerkhof, L.J. (2005) Phylogeography of sulfate-reducing bacteria among disturbed sediments, disclosed by analysis of the dissimilatory sulfite reductase genes (dsrAB). Appl Environ Microbiol 71 : 1004 1011. (Pubitemid 40223589)
46. Plugge, C.M., Balk, M. Stams, A.J. (2002) Desulfotomaculum thermobenzoicum subsp. thermosyntrophicum subsp. nov., a thermophilic, syntrophic, propionate-oxidizing, spore-forming bacterium. Int J Syst Evol Microbiol 52 : 391 399. (Pubitemid 34262633)
47. Purdy, K.J., Nedwell, D.B., Embley, T.M. Takii, S. (2001) Use of 16S rRNA-targeted oligonucleotide probes to investigate the distribution of sulfate-reducing bacteria in estuarine sediments. FEMS Microbiol Ecol 36 : 165 168. (Pubitemid 32635237)
48. Quéric, N.V., Soltwedel, T. Arntz, W.E. (2004) Application of a rapid direct viable count method to deep-sea sediment bacteria. J Microbiol Methods 57 : 351 367. (Pubitemid 38595302)
49. Ravenschlag, K., Sahm, K., Knoblauch, C., Jørgensen, B.B. Amann, R. (2000) Community structure, cellular rRNA content and activity of sulfate reducing bacteria in marine arctic sediments. Appl Environ Microbiol 66 : 3592 3602. (Pubitemid 30624602)
50. Rudi, K., Moen, B., Drømtrop, S.M. Holck, A.L. (2005) Use of Ethidium Monoazide and PCR in combination for quantification of viable and dead cells in complex samples. Appl Environ Microbiol 71 : 1018 1024. (Pubitemid 40223590)
51. Sahm, K., MacGregor, B.J., Jørgensen, B.B. Stahl, D.A. (1999) Sulphate reduction and vertical distribution of sulphate-reducing bacteria quantified by rRNA slot-blot hybridization in a coastal marine sediment. Environ Microbiol 1 : 65 74. (Pubitemid 129640029)
52. Sambrook, J., Fritsch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY, USA : Cold Spring Harbor Laboratory Press.
53. Schink, B. (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbol Mol Biol Rev 61 : 262 280. (Pubitemid 27283803)
54. Singleton, D.R., Furlong, M.A., Rathbun, S.L. Whitman, W.B. (2001) Quantitative comparisons of 16SrRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67 : 4373 4376. (Pubitemid 33641744)
55. 0 in coastal marine sediments. Limnol Oceanogr 34 : 793 806. (Pubitemid 19306183)
56. Thomsen, T.R., Finster, K. Ramsing, N.B. (2001) Biogeochemical and molecular signatures of anaerobic methane oxidation in a marine sediment. Appl Environ Microbiol 67 : 1646 1656. (Pubitemid 33644935)
57. Vandieken, V., Knoblauch, C. Jørgensen, B.B. (2006) Desulfovibrio frigidus sp. nov. and Desulfovibrio ferrireducens sp. nov., two psychrotolerant bacteria isolated from Arctic fjord sediments (Svalbard) with the ability to reduce Fe(III). Int J Syst Evol Microbiol 56 : 681 685. (Pubitemid 43820845)
58. Vetriani, C., Tran, H.V. Kerkhof, L.J. (2003) Fingerprinting microbial assemblages from the oxic/anoxic chemocline of the Black Sea. Appl Environ Microbiol 69 : 6481 6488. (Pubitemid 37420180)
59. Wagner, M., Loy, A., Klein, M., Lee, N., Ramsing, N.B., Stahl, D.A. Friedrich, M.W. (2005) Functional marker genes for identification of sulfate-reducing prokaryotes. Methods Enzymol 397 : 469 489. (Pubitemid 41562916)
60. Wallrabenstein, C., Hauschild, E. Schink, B. (1994) Pure culture and cytological properties of Syntrophobacter wolinii. FEMS Microbiol Lett 123 : 249 254. (Pubitemid 24323007)
61. Widdel, F. Bak, F. (1992) Gram-negative mesophilic sulfate-reducing bacteria. In The Prokaryotes: A Handbook on the Biology of Bacteria, Ecophysiology, Identification, 2nd edn. Balows, A., Truper, H.G., Dworkin, M., Harder, W. Schleifer, K.-H. (eds). New York, NY, USA : Springer Verlag, pp. 3353 3378.
62. Zverlov, V., Klein, M., Lücker, S., Friedrich, M.W., Kellermann, J., Stahl, D.A., et al. (2005) Lateral gene transfer of dissimilatory (bi)sulfite reductase revisited. J Bacteriol 187 : 2203 2208. (Pubitemid 40316252)