Molecular analysis of the diversity of the sulfide : quinone reductase () gene in sediment environments Free

Abstract

Our newly designed primers were evaluated for the molecular analysis of specific groups of the gene encoding sulfide : quinone reductase (SQR) in sediment environments. Based on the phylogenetic analysis, we classified the sequences into six groups. PCR primers specific for each group were developed. We successfully amplified -like gene sequences related to groups 1, 2 and 4 from diverse sediments including a marine sediment (SW), a tidal flat (TS), a river sediment (RS) and a lake sediment (FW). We recovered a total of 82 unique phylotypes (based on a 95 % amino acid sequence similarity cutoff) from 243 individual -like gene sequences. Phylotype richness varied widely among the groups of -like gene sequences (group 1>group 2>group 4) and sediments (SW>TS>RS>FW). Most of the -like gene sequences were affiliated with the clade and were distantly related to the reference gene sequences from cultivated strains (less than ∼80 % amino acid sequence similarity). Unique -like gene sequences were associated with individual sediment samples in groups 1 and 2. This molecular tool has also enabled us to detect -like genes in a sulfur-oxidizing enrichment from marine sediments. Collectively, our results support the presence of previously unrecognized gene-containing micro-organisms that play important roles in the global biogeochemical cycle of sulfur.

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2008-10-01
2024-03-29
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References

  1. Abascal F., Zardoya R., Posada D. 2005; ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105
    [Google Scholar]
  2. Altekar G., Dwarkadas S., Huelsenbeck J. P., Ronquist F. 2004; Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20:407–415
    [Google Scholar]
  3. Arieli B., Shahak Y., Taglicht D., Hauska G., Padan E. 1994; Purification and characterization of sulfide-quinone reductase, a novel enzyme driving anoxygenic photosynthesis in Oscillatoria limnetica . J Biol Chem 269:5705–5711
    [Google Scholar]
  4. Beiko R. G., Keith J. M., Harlow T. J., Ragan M. A. 2006; Searching for convergence in phylogenetic Markov chain Monte Carlo. Syst Biol 55:553–565
    [Google Scholar]
  5. Braker G., Zhou J., Wu L., Devol A. H., Tiedje J. M. 2000; Nitrite reductase genes ( nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in pacific northwest marine sediment communities. Appl Environ Microbiol 66:2096–2104
    [Google Scholar]
  6. Brettar I., Labrenz M., Flavier S., Botel J., Kuosa H., Christen R., Hofle M. G. 2006; Identification of a Thiomicrospira denitrificans-like epsilonproteobacterium as a catalyst for autotrophic denitrification in the central Baltic Sea. Appl Environ Microbiol 72:1364–1372
    [Google Scholar]
  7. Brune D. C. 1995; Sulfur compounds as photosynthetic electron donors. In Anoxygenic Photosynthetic Bacteria pp 847–870 Edited by Blankenship R. E., Madigan M. T., Bauer C. E. Dordrecht: Kluwer;
    [Google Scholar]
  8. Campbell B. J., Engel A. S., Porter M. L., Takai K. 2006; The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468
    [Google Scholar]
  9. Cottrell M. T., Cary S. C. 1999; Diversity of dissimilatory bisulfite reductase genes of bacteria associated with the deep-sea hydrothermal vent polychaete annelid Alvinella pompejana . Appl Environ Microbiol 65:1127–1132
    [Google Scholar]
  10. Cytryn E., van Rijn J., Schramm A., Gieseke A., de Beer D., Minz D. 2005; Identification of bacteria potentially responsible for oxic and anoxic sulfide oxidation in biofilters of a recirculating mariculture system. Appl Environ Microbiol 71:6134–6141
    [Google Scholar]
  11. Dahl C., Prange A., Steudel R. 2002 Natural Polymeric Sulfur Compounds Weinheim: Wiley-VCH;
    [Google Scholar]
  12. Deckert G., Warren P. V., Gaasterland T., Young W. G., Lenox A. L., Graham D. E., Overbeek R., Snead M. A., Keller M. other authors 1998; The complete genome of the hyperthermophilic bacterium Aquifex aeolicus . Nature 392:353–358
    [Google Scholar]
  13. Detmers J., Schulte U., Strauss H., Kuever J. 2001; Sulfate reduction at a lignite seam: microbial abundance and activity. Microb Ecol 42:238–247
    [Google Scholar]
  14. Duperron S., Bergin C., Zielinski F., Blazejak A., Pernthaler A., McKiness Z. P., DeChaine E., Cavanaugh C. M., Dubilier N. 2006; A dual symbiosis shared by two mussel species, Bathymodiolus azoricus and Bathymodiolus puteoserpentis ( Bivalvia: Mytilidae), from hydrothermal vents along the northern Mid-Atlantic Ridge. Environ Microbiol 8:1441–1447
    [Google Scholar]
  15. Fennell D. E., Rhee S. K., Ahn Y. B., Haggblom M. M., Kerkhof L. J. 2004; Detection and characterization of a dehalogenating microorganism by terminal restriction fragment length polymorphism fingerprinting of 16S rRNA in a sulfidogenic, 2-bromophenol-utilizing enrichment. Appl Environ Microbiol 70:1169–1175
    [Google Scholar]
  16. Friedrich C. G. 1998 Physiology and Genetics of Sulfur-Oxidizing Bacteria London: Academic Press;
    [Google Scholar]
  17. Furne J., Springfield J., Koenig T., DeMaster E., Levitt M. D. 2001; Oxidation of hydrogen sulfide and methanethiol to thiosulfate by rat tissues: a specialized function of the colonic mucosa. Biochem Pharmacol 62:255–259
    [Google Scholar]
  18. Good I. J. 1953; The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264
    [Google Scholar]
  19. Goubern M., Andriamihaja M., Nubel T., Blachier F., Bouillaud F. 2007; Sulfide, the first inorganic substrate for human cells. FASEB J 21:1699–1706
    [Google Scholar]
  20. Griesbeck C., Gunter H., Schutz M. 2000 Biological Sulfide Oxidation: Sulfide-Quinone Reductase (SQR), the Primary Reaction Trivandrum, India: Research Signpost;
    [Google Scholar]
  21. Griesbeck C., Schutz M., Schodl T., Bathe S., Nausch L., Mederer N., Vielreicher M., Hauska G. 2002; Mechanism of sulfide-quinone reductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41:11552–11565
    [Google Scholar]
  22. Jorgensen B. B. 1982; Ecology of the bacteria of the sulphur cycle with special reference to anoxic–oxic interface environments. Philos Trans R Soc Lond B Biol Sci 298:543–561
    [Google Scholar]
  23. Kandeler E., Deiglmayr K., Tscherko D., Bru D., Philippot L. 2006; Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72:5957–5962
    [Google Scholar]
  24. Kusai A., Yamanaka T. 1973a; Cytochrome c (553, Chlorobium thiosulfatophilum) is a sulphide-cytochrome c reductase. FEBS Lett 34:235–237
    [Google Scholar]
  25. Kusai A., Yamanaka T. 1973b; A novel function of cytochrome c (555, Chlorobium thiosulfatophilum) in oxidation of thiosulfate. Biochem Biophys Res Commun 51:107–112
    [Google Scholar]
  26. Kusai K., Yamanaka T. 1973c; The oxidation mechanisms of thiosulphate and sulphide in Chlorobium thiosulphatophilum: roles of cytochrome c-551 and cytochrome c-553. Biochim Biophys Acta 325:304–314
    [Google Scholar]
  27. Lee R. W., Kraus D. W., Doeller J. E. 1996; Sulfide-stimulation of oxygen consumption rate and cytochrome reduction in gills of the estuarine mussel Geukensia demissa . Biol Bull 191:421–430
    [Google Scholar]
  28. Lyric R. M., Suzuki I. 1970a; Enzymes involved in the metabolism of thiosulfate by Thiobacillus thioparus. 3. Properties of thiosulfate-oxidizing enzyme and proposed pathway of thiosulfate oxidation. Can J Biochem 48:355–363
    [Google Scholar]
  29. Lyric R. M., Suzuki I. 1970b; Enzymes involved in the metabolism of thiosulfate by Thiobacillus thioparus. II. Properties of adenosine-5′-phosphosulfate reductase. Can J Biochem 48:344–354
    [Google Scholar]
  30. Lyric R. M., Suzuki I. 1970c; Enzymes involved in the metabolism of thiosulfate by Thiobacillus thioparus. I. Survey of enzymes and properties of sulfite : cytochrome c oxidoreductase. Can J Biochem 48:334–343
    [Google Scholar]
  31. Newton I. L., Woyke T., Auchtung T. A., Dilly G. F., Dutton R. J., Fisher M. C., Fontanez K. M., Lau E., Stewart F. J. other authors 2007; The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315:998–1000
    [Google Scholar]
  32. Nubel T., Klughammer C., Huber R., Hauska G., Schutz M. 2000; Sulfide : quinone oxidoreductase in membranes of the hyperthermophilic bacterium Aquifex aeolicus (VF5. Arch Microbiol 173:233–244
    [Google Scholar]
  33. Nuin P. A., Wang Z., Tillier E. R. 2006; The accuracy of several multiple sequence alignment programs for proteins. BMC Bioinformatics 7:471
    [Google Scholar]
  34. Oeschger R., Vismann B. 1994; Sulphide tolerance in Heteromastus filiformis ( Polychaeta): mitochondrial adaptations. Ophelia 40:147–158
    [Google Scholar]
  35. Park S. J., Kang C. H., Rhee S. K. 2006; Characterization of the microbial diversity in a Korean Solar Saltern by 16S rRNA gene analysis. J Microbiol Biotechnol 16:1640–1645
    [Google Scholar]
  36. Posada D., Buckley T. R. 2004; Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808
    [Google Scholar]
  37. Ravenschlag K., Sahm K., Pernthaler J., Amann R. 1999; High bacterial diversity in permanently cold marine sediments. Appl Environ Microbiol 65:3982–3989
    [Google Scholar]
  38. Reinartz M., Tschape T., Bruser T., Truper H. G., Dahl C. 1998; Sulfide oxidation in the phototrophic bacterium Chromatium vinosum . Arch Microbiol 170:59–68
    [Google Scholar]
  39. Rhee S. K., Lee G. M., Yoon J. H., Park Y. H., Bae H. S., Lee S. T. 1997; Anaerobic and aerobic degradation of pyridine by a newly isolated denitrifying bacterium. Appl Environ Microbiol 63:2578–2585
    [Google Scholar]
  40. Ronquist F., Huelsenbeck J. P. 2003; MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
    [Google Scholar]
  41. Ruepp A., Graml W., Santos-Martinez M. L., Koretke K. K., Volker C., Mewes H. W., Frishman D., Stocker S., Lupas A. N., Baumeister W. 2000; The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum . Nature 407:508–513
    [Google Scholar]
  42. Scala D. J., Kerkhof L. J. 1998; Nitrous oxide reductase ( nosZ) gene-specific PCR primers for detection of denitrifiers and three nosZ genes from marine sediments. FEMS Microbiol Lett 162:61–68
    [Google Scholar]
  43. Schmidt H. A., Strimmer K., Vingron M., von Haeseler A. 2002; tree-puzzle: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504
    [Google Scholar]
  44. Schutz M., Shahak Y., Padan E., Hauska G. 1997; Sulfide-quinone reductase from Rhodobacter capsulatus. Purification, cloning, and expression. J Biol Chem 272:9890–9894
    [Google Scholar]
  45. Schutz M., Klughammer C., Griesbeck C., Quentmeier A., Friedrich C. G., Hauska G. 1998; Sulfide-quinone reductase activity in membranes of the chemotrophic bacterium Paracoccus denitrificans GB17. Arch Microbiol 170:353–360
    [Google Scholar]
  46. Schutz M., Maldener I., Griesbeck C., Hauska G. 1999; Sulfide-quinone reductase from Rhodobacter capsulatus: requirement for growth, periplasmic localization, and extension of gene sequence analysis. J Bacteriol 181:6516–6523
    [Google Scholar]
  47. Scott K. M., Sievert S. M., Abril F. N., Ball L. A., Barrett C. J., Blake R. A., Boller A. J., Chain P. S., Clark J. A. other authors 2006; The genome of deep-sea vent chemolithoautotroph Thiomicrospira crunogena XCL-2. PLoS Biol 4:e383
    [Google Scholar]
  48. Shahak Y., Arieli B., Padan E., Hauska G. 1992; Sulfide quinone reductase (SQR) activity in Chlorobium . FEBS Lett 299:127–130
    [Google Scholar]
  49. Shahak Y., Schuetz M., Bronstein M., Hauska G., Padan E. 1999; Sulfide-dependent anoxygenic photosynthesis in prokaryotes: sulfide-quinone reductase (SQR). In The Phototrophic Prokaryotes pp 217–228 Edited by Peschek G. A., Loeffelhardt W., Schmetterer G. New York: Plenum;
    [Google Scholar]
  50. She Q., Singh R. K., Confalonieri F., Zivanovic Y., Allard G., Awayez M. J., Chan-Weiher C. C., Clausen I. G., Curtis B. A. other authors 2001; The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci U S A 98:7835–7840
    [Google Scholar]
  51. Smith C. J., Nedwell D. B., Dong L. F., Osborn A. M. 2007; Diversity and abundance of nitrate reductase ( narG and napA), and nitrite reductase ( nirS and nrfA) genes and transcripts in estuarine sediments. Appl Environ Microbiol 73:3612–3622
    [Google Scholar]
  52. Sorensen J., Christensen D., Jorgensen B. B. 1981; Volatile fatty acids and hydrogen as substrates for sulfate-reducing bacteria in anaerobic marine sediment. Appl Environ Microbiol 42:5–11
    [Google Scholar]
  53. Theissen U., Hoffmeister M., Grieshaber M., Martin W. 2003; Single eubacterial origin of eukaryotic sulfide : quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Mol Biol Evol 20:1564–1574
    [Google Scholar]
  54. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
    [Google Scholar]
  55. Vande Weghe J. G., Ow W. D. 1999; A fission yeast gene for mitochondrial sulfide oxidation. J Biol Chem 274:13250–13257
    [Google Scholar]
  56. Weisburg W. G., Barns S. M., Pelletier D. A., Lane D. J. 1991; 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
    [Google Scholar]
  57. Yong R., Searcy D. G. 2001; Sulfide oxidation coupled to ATP synthesis in chicken liver mitochondria. Comp Biochem Physiol B Biochem Mol Biol 129:129–137
    [Google Scholar]
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