Novel groups of Gammaproteobacteria catalyse sulfur oxidation and carbon fixation in a coastal, intertidal sediment

Environmental Microbiology

Volumn 13, Issue 3, 2011, Pages 758-774

  Lenk, Sabine ^a   Arnds, Julia ^a   Zerjatke, Katrice ^a   Musat, Niculina ^a   Amann, Rudolf ^a   Mußmann, Marc ^a  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN SULFITE REDUCTASE; RNA 16S; SULFIDE; SULFUR;

ARTICLE; BIOCATALYSIS; CARBON CYCLE; CLASSIFICATION; GAMMAPROTEOBACTERIA; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHYLOGENY; RNA GENE; SEDIMENT;

BIOCATALYSIS; CARBON CYCLE; GAMMAPROTEOBACTERIA; GENES, RRNA; GEOLOGIC SEDIMENTS; HYDROGENSULFITE REDUCTASE; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S; SULFIDES; SULFUR;

BACTERIA (MICROORGANISMS); GAMMAPROTEOBACTERIA; OLIGOBRACHIA; PROKARYOTA; TUBICOLAE; UNCULTURED GAMMA PROTEOBACTERIUM;

EID: 79952083631     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02380.x     Document Type: Article

References (87)

1. Aida, M., Kanemori, M., Kubota, N., Matada, M., Sasayama, Y., and Fukumori, Y. (2008) Distribution and population of free-living cells related to endosymbiont a harbored in Oligobrachia mashikoi (a siboglinid polychaete) inhabiting Tsukumo Bay. Microbes Environ 23: 81-88.
2. Alonso, C., and Pernthaler, J. (2005) Incorporation of glucose under anoxic conditions by bacterioplankton from coastal North Sea surface waters. Appl Environ Microbiol 71: 1709-1716.
3. Al-Raei, A.M., Bosselmann, K., Bottcher, M.E., Hespenheide, B., and Tauber, F. (2009) Seasonal dynamics of microbial sulfate reduction in temperate intertidal surface sediments: controls by temperature and organic matter. Ocean Dyn 59: 351-370.
4. Amann, R.I., Binder, B.J., Olson, R.J., Chisholm, S.W., Devereux, R., and Stahl, D.A. (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Environ Microbiol 56: 1919-1925.
5. Asami, H., Aida, M., and Watanabe, K. (2005) Accelerated sulfur cycle in coastal marine sediment beneath areas of intensive shellfish aquaculture. Appl Environ Microbiol 71: 2925-2933.
6. Billerbeck, M., Werner, U., Polerecky, L., Walpersdorf, E., deBeer, D., and Huettel, M. (2006) Surficial and deep pore water circulation governs spatial and temporal scales of nutrient recycling in intertidal sand flat sediment. Mar Ecol Prog Ser 326: 61-76.
7. Bowman, J.P., McCammon, S.A., Gibson, J.A.E., Robertson, L., and Nichols, P.D. (2003) Prokaryotic metabolic activity and community structure in Antarctic continental shelf sediments. Appl Environ Microbiol 69: 2448-2462.
8. Brinkhoff, T., and Muyzer, G. (1997) Increased species diversity and extended habitat range of sulfur-oxidizing Thiomicrospira spp. Appl Environ Microbiol 63: 3789-3796.
9. Brinkhoff, T., Santegoeds, C.M., Sahm, K., Kuever, J., and Muyzer, G. (1998) A polyphasic approach to study the diversity and vertical distribution of sulfur-oxidizing Thiomicrospira species in coastal sediments of the German Wadden Sea. Appl Environ Microbiol 64: 4650-4657.
10. Brinkhoff, T., Muyzer, G., Wirsen, C.O., and Kuever, J. (1999) Thiomicrospira kuenenii sp. nov. Thiomicrospira frisia sp. nov., two mesophilic obligately chemolithoautotrophic sulfur-oxidizing bacteria isolated from an intertidal mud flat. Int J Syst Bacteriol 49: 385-392.
11. Bruechert, V., Jorgensen, B.B., Neumann, K., Riechmann, D., Schlosser, M., and Schulz, H. (2003) Regulation of bacterial sulfate reduction and hydrogen sulfide fluxes in the central Namibian coastal upwelling zone. Geochim Cosmochim Acta 67: 4505-4518.
12. Buehring, S.I., Elvert, M., and Witte, U. (2005) The microbial community structure of different permeable sandy sediments characterized by the investigation of bacterial fatty acids and fluorescence in situ hybridization. Environ Microbiol 7: 281-293.
13. Campbell, B.J., Engel, A.S., Porter, M.L., and Takai, K. (2006) The versatile Epsilonproteobacteria: key players in sulphidic habitats. Nat Rev Micro 4: 458-468.
14. Dahl, C., Engels, S., Pott-Sperling, A.S., Schulte, A., Sander, J., Luebbe, J., etal. (2005) Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. J Bacteriol 187: 1392-1404.
15. Daims, H., Bruhl, A., Amann, R., Schleifer, K.H., and Wagner, M. (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22: 434-444.
16. Eilers, H., Pernthaler, J., Peplies, J., Glockner, F.O., Gerdts, G., and Amann, R. (2001) Isolation of novel pelagic bacteria from the German bight and their seasonal contributions to surface picoplankton. Appl Environ Microbiol 67: 5134-5142.
17. Feng, B.-W., Li, X.-R., Wang, J.-H., Hu, Z.-Y., Meng, H., Xiang, L.-Y., and Quan, Z.-X. (2009) Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea. FEMS Microbiol Ecol 70: 80-92.
18. Fuchs, B.M., Spring, S., Teeling, H., Quast, C., Wulf, J., Schattenhofer, M., etal. (2007) Characterization of a marine gammaproteobacterium capable of aerobic anoxygenic photosynthesis. Proc Natl Acad Sci USA 104: 2891-2896.
19. Gao, H., Schreiber, F., Collins, G., Jensen, M.M., Kostka, J.E., Lavik, G., etal. (2009) Aerobic denitrification in permeable Wadden Sea sediments. ISME J 4: 417-426.
20. Gevertz, D., Telang, A.J., Voordouw, G., and Jenneman, G.E. (2000) Isolation and characterization of strains CVO and FWKOB, two novel nitrate-reducing, sulfide-oxidizing bacteria isolated from oil field brine. Appl Environ Microbiol 66: 2491-2501.
21. Gillan, D.C., and Pernet, P. (2007) Adherent bacteria in heavy metal contaminated marine sediments. Biofouling 23: 1-13.
22. Good, I.J. (1953) The population frequencies of species and the estimation to the population parameters. Biometrika 40: 237-264.
23. Grabovich, M.Y., Muntyan, M.S., Lebedeva, V.Y., Ustiyan, V.S., and Dubinina, G.A. (1999) Lithoheterotrophic growth and electron transfer chain components of the filamentous gliding bacterium Leucothrix mucor DSM 2157 during oxidation of sulfur compounds. FEMS Microbiol Lett 178: 155-161.
24. Grote, J., Labrenz, M., Pfeiffer, B., Jost, G., and Jurgens, M. (2007) Quantitative distributions of Epsilonproteobacteria and a Sulfurimonas subgroup in pelagic redoxclines of the central Baltic sea. Appl Environ Microbiol 73: 7155-7161.
25. Heijs, S.K., Jonkers, H.M., van Gemerden, H., Schaub, B.E.M., and Stal, L.J. (1999) The buffering capacity towards free sulphide in sediments of a coastal lagoon (Bassin d'Arcachon, France) - the relative importance of chemical and biological processes. Estuar Coast Shelf Sci 49: 21-35.
26. Hong, S.H., Bunge, J., Jeon, S.O., and Epstein, S.S. (2006) Predicting microbial species richness. Proc Natl Acad Sci USA 103: 117-122.
27. Huber, T., Faulkner, G., and Hugenholtz, P. (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319.
28. Huelsenbeck, J.P., and Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
29. Ishii, K., Mussmann, M., MacGregor, B.J., and Amann, R. (2004) An improved fluorescence in situ hybridization protocol for the identification of Bacteria and Archaea in marine sediments. FEMS Microbiol Ecol 50: 203-212.
30. Jansen, S., Walpersdorf, E., Werner, U., Billerbeck, M., Böttcher, M., and de Beer, D. (2009) Functioning of intertidal flats inferred from temporal and spatial dynamics of O2, H2S and pH in their surface sediment. Ocean Dyn 59: 317-332.
31. Jørgensen, B.B. (1982) Mineralization of organic matter in the sea bed - the role of sulphate reduction. Nature 296: 643-645.
32. Jørgensen, B.B., and Nelson, D.C. (2004) Sulfide oxidation in marine sediments: geochemistry meets microbiology. In Sulfur Biogeochemistry - Past and Present. Amend, J.P., Edwards, K.J., and Lyons, T.W. (eds). Boulder, CO, USA: Geological Society of America, pp. 63-81.
33. Jost, G., Zubkov, M.V., Yakushev, E., Labrenz, M., and Jurgens, K. (2008) High abundance and dark CO2 fixation of chemolithoautotrophic prokaryotes in anoxic waters of the Baltic Sea. Limnol Oceanogr 53: 14-22.
34. Juretschko, S. (2000) Mikrobielle Populationsstruktur und -dynamik in einer nitrifizierenden/denitrifizierenden Belebtschlammanlage. PhD Thesis. Munich, Germany: Technical University Munich.
35. Kamp, A., Stief, P., and Schulz-Vogt, H.N. (2006) Anaerobic sulfide oxidation with nitrate by a freshwater Beggiatoa enrichment culture. Appl Environ Microbiol 72: 4755-4760.
36. Kamyshny, A., and Ferdelman, T.G. (2007) Dynamics of zero-valent sulfur species, including polysulfides, in Wadden Sea tidal flat pools. Geochim Cosmochim Acta 71: A461-A461.
37. Knittel, K., Boetius, A., Lemke, A., Eilers, H., Lochte, K., Pfannkuche, O., etal. (2003) Activity, distribution and diversity of sulfate reducers and other bacteria in sediments above gas hydrate (Cascadia margin, Oregon). Geomicrobiol J 20: 269-294.
38. Kuenen, J.G., and Veldkamp, H. (1972) Thiomicrospira pelophila gen. n. sp. n., a new obligately chemolithotrophic colourless sulfur bacterium. Antonie Van Leeuwenhoek 38: 241-256.
39. Lavik, G., Stuhrmann, T., Bruchert, V., Van der Plas, A., Mohrholz, V., Lam, P., etal. (2009) Detoxification of sulphidic African shelf waters by blooming chemolithotrophs. Nature 457: 581-584.
40. Lin, X., Wakeham, S.G., Putnam, I.F., Astor, Y.M., Scranton, M.I., Chistoserdov, A.Y., and Taylor, G.T. (2006) Comparison of vertical distributions of prokaryotic assemblages in the anoxic Cariaco Basin and Black Sea by use of fluorescence in situ hybridization. Appl Environ Microbiol 72: 2679-2690.
41. Llobet-Brossa, E., Rossello-Mora, R., and Amann, R. (1998) Microbial community composition of Wadden Sea sediments as revealed by fluorescence in situ hybridization. Appl Environ Microbiol 64: 2691-2696.
42. Loesekann, T., Robador, A., Niemann, H., Knittel, K., Boetius, A., and Dubilier, N. (2008) Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an Arctic cold seep (Haakon Mosby Mud Volcano, Barents Sea). Environ Microbiol 10: 3237-3254.
43. Loy, A., Duller, S., Baranyi, C., Mussmann, M., Ott, J., Sharon, I., etal. (2009) Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes. Environ Microbiol 11: 289-299.
44. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, etal. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
45. Macalady, J.L., Lyon, E.H., Koffman, B., Albertson, L.K., Meyer, K., Galdenzi, S., and Mariani, S. (2006) Dominant microbial populations in limestone-corroding stream biofilms, Frasassi cave system, Italy. Appl Environ Microbiol 72: 5596-5609.
46. Manz, W., Amann, R., Ludwig, W., Wagner, M., and Schleifer, K.-H. (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15: 593-600.
47. Meyer, B., and Kuever, J. (2007a) Molecular analysis of the diversity of sulfate-reducing and sulfur-oxidizing prokaryotes in the environment, using aprA as functional marker gene. Appl Environ Microbiol 73: 7664-7679.
48. Meyer, B., and Kuever, J. (2007b) Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5'-phosphosulfate reductase-encoding genes (aprBA) among sulfur oxidizing prokaryotes. Microbiology 153: 3478-3498.
49. Meyer, B., Imhoff, J.F., and Kuever, J. (2007) Molecular analysis of the distribution and phylogeny of the soxB gene among sulfur-oxidizing bacteria - evolution of the Sox sulfur oxidation enzyme system. Environ Microbiol 9: 2957-2977.
50. Musat, N., Werner, U., Knittel, K., Kolb, S., Dodenhof, T., van Beusekom, J.E.E., etal. (2006) Microbial community structure of sandy intertidal sediments in the North Sea, Sylt-Romo Basin, Wadden Sea. Syst Appl Microbiol 29: 333-348.
51. Musat, N., Halm, H., Winterholler, B., Hoppe, P., Peduzzi, S., Hillion, F., etal. (2008) A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. Proc Natl Acad Sci USA 105: 17861-17866.
52. Mussmann, M., Schulz, H.N., Strotmann, B., Kjaer, T., Nielsen, L.P., Rossello-Mora, R.A., etal. (2003) Phylogeny and distribution of nitrate-storing Beggiatoa spp. in coastal marine sediments. Environ Microbiol 5: 523-533.
53. Mussmann, M., Ishii, K., Rabus, R., and Amann, R. (2005a) Diversity and vertical distribution of cultured and uncultured Deltaproteobacteria in an intertidal mud flat of the Wadden Sea. Environ Microbiol 7: 405-418.
54. Mussmann, M., Richter, M., Lombardot, T., Meyerdierks, A., Kuever, J., Kube, M., etal. (2005b) Clustered genes related to sulfate respiration in uncultured prokaryotes support the theory of their concomitant horizontal transfer. J Bacteriol 187: 7126-7137.
55. Mussmann, M., Hu, F.Z., Richter, M., de Beer, D., Preisler, A., Jørgensen, B., etal. (2007) Insights into the genome of large sulfur bacteria revealed by analysis of single filaments. PLoS Biol 5: 1923-1937.
56. Muyzer, G., Teske, A., Wirsen, C.O., and Jannasch, H.W. (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164: 165-172.
57. Nelson, D.C., and Jannasch, H.W. (1983) Chemoautotrophic growth of a marine Beggiatoa in sulfide-gradient cultures. Arch Microbiol 136: 262-269.
58. Nielsen, L.P., Risgaard-Petersen, N., Fossing, H., Christensen, P.B., and Sayama, M. (2010) Electric currents couple spatially separated biogeochemical processes in marine sediment. Nature 463: 1071-1074.
59. Pernthaler, A., and Amann, R. (2004) Simultaneous fluorescence in situ hybridization of mRNA and rRNA in environmental bacteria. Appl Environ Microbiol 70: 5426-5433.
60. Petri, R., Podgorsek, L., and Imhoff, J.F. (2001) Phylogeny and distribution of the soxB gene among thiosulfate-oxidizing bacteria. FEMS Microbiol Lett 197: 171-178.
61. Pham, V.H., Yong, J.J., Park, S.J., Yoon, D.N., Chung, W.H., and Rhee, S.K. (2008) Molecular analysis of the diversity of the sulfide: quinone reductase (sqr) gene in sediment environments. Microbiology 154: 3112-3121.
62. Podgorsek, L., and Imhoff, J.F. (1999) Tetrathionate production by sulfur oxidizing bacteria and the role of tetrathionate in the sulfur cycle of Baltic Sea sediments. Aquat Microb Ecol 17: 255-265.
63. Pott, A.S., and Dahl, C. (1998) Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology 144: 1881-1894.
64. Preisler, A., de Beer, D., Lichtschlag, A., Lavik, G., Boetius, A., and Jørgensen, B.B. (2007) Biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment. ISME J 1: 341-353.
65. Pruesse, E., Quast, C., Knittel, K., Fuchs, B.M., Ludwig, W.G., Peplies, J., and Glockner, F.O. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
66. Ravenschlag, K., Sahm, K., Pernthaler, J., and Amann, R. (1999) High bacterial diversity in permanently cold marine sediments. Appl Environ Microbiol 65: 3982-3989.
67. Ravenschlag, K., Sahm, K., and Amann, R. (2001) Quantitative molecular analysis of the microbial community in marine Arctic sediments (Svalbard). Appl Environ Microbiol 67: 387-395.
68. Rinke, C., Schmitz-Esser, S., Stoecker, K., Nussbaumer, A.D., Molnar, D.A., Vanura, K., etal. (2006) 'Candidatus Thiobios zoothamnicoli' an ectosymbiotic bacterium covering the giant marine ciliate Zoothamnium niveum. Appl Environ Microbiol 72: 2014-2021.
69. Robidart, J.C., Bench, S.R., Feldman, R.A., Novoradovsky, A., Podell, S.B., Gaasterland, T., etal. (2008) Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ Microbiol 10: 727-737.
70. Sandrin, T.R., Herman, D.C., and Maier, R.M. (2008) Physiological methods. In Environmental Microbiology, 11th edn. Maier, R.M., Pepper, I.L., and Gerba, C.P. (eds). San Diego, CA, USA: Elsevier Science, p. 195.
71. Schaub, B.E.M., and Gemerden, H. (1996) Sulfur bacteria in sediments of two coastal ecosystems: the Bassin d'Arcachon and the Etang du Prévost, France. Hydrobiologia 329: 199-210.
72. Schloss, P.D., and Handelsman, J. (2005) Introducing dotur, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501-1506.
73. Schramm, A., Fuchs, B.M., Nielsen, J.L., Tonolla, M., and Stahl, D.A. (2002) Fluorescence in situ hybridization of 16S rRNA gene clones (Clone-FISH) for probe validation and screening of clone libraries. Environ Microbiol 4: 713-720.
74. 2 uptake and fixation by endosymbiotic chemoautotrophs from the bivalve Solemya velum. Appl Environ Microbiol 73: 1174-1179.
75. Snaidr, J., Amann, R., Huber, I., Ludwig, W., and Schleifer, K.-H. (1997) Phylogenetic analysis and in situ identification of bacteria in activated sludge. Appl Environ Microbiol 63: 2884-2896.
76. Sorokin, D.Y., Tourova, T.P., and Muyzer, G. (2005) Citreicella thiooxidans gen. nov., sp. nov., a novel lithoheterotrophic sulfur-oxidizing bacterium from the Black Sea. Syst Appl Microbiol 28: 679-687.
77. Stamatakis, A., Hoover, P., and Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57: 758-771.
78. Timmer-Ten Hoor, A. (1975) A new type of thiosulfate oxidizing, nitrate reducing microorganism: Thiomicrospira denitrificans sp. nov. Neth J Sea Res 9: 344-350.
79. Wagner-Doebler, I., and Biebl, H. (2006) Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol 60: 255-280.
80. Wallner, G., Amann, R., and Beisker, W. (1993) Optimizing flourescent in situ-hybridization with rRNA-targeted oligonulcleotide probes for flow cytometric identification of microorganisms. Cytometry 14: 136-143.
81. Walsh, D.A., Zaikova, E., Howes, C.G., Song, Y.C., Wright, J.J., Tringe, S.G., etal. (2009) Metagenome of a versatile chemolithoautotroph from expanding oceanic dead zones. Science 326: 578-582.
82. Wirsen, C.O., Sievert, S.M., Cavanaugh, C.M., Molyneaux, S.J., Ahmad, A., Taylor, L.T., etal. (2002) Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur. Appl Environ Microbiol 68: 316-325.
83. Woyke, T., Teeling, H., Ivanova, N.N., Huntemann, M., Richter, M., Gloeckner, F.O., etal. (2006) Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443: 950-955.
84. Yan, S. (2009) Molecular ecology of the NOR5/OM60 group of Gammaproteobacteria. Masters Thesis. Fachbereich für Chemie und Biologie. Bremen, Germany: University of Bremen.
85. Yan, S., Fuchs, B.M., Lenk, S., Harder, J., Wulf, J., Jiao, N.-Z., and Amann, R. (2009) Biogeography and phylogeny of the NOR5/OM60 clade of Gammaproteobacteria. Syst Appl Microbiol 32: 124-139.
86. Yilmaz, L.S., and Noguera, D.R. (2004) Mechanistic approach to the problem of hybridization efficiency in fluorescent in situ hybridization. Appl Environ Microbiol 70: 7126-7139.
87. Zhou, J., Bruns, M.A., and Tiedje, J.M. (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62: 316-322.