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Volume 153, Issue 10

Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5′-phosphosulfate reductase-encoding genes () among sulfur-oxidizing prokaryotes Free

Abstract

Dissimilatory adenosine-5′-phosphosulfate (APS) reductase (AprBA) is a key enzyme of the dissimilatory sulfate-reduction pathway. Homologues have been found in photo- and chemotrophic sulfur-oxidizing prokaryotes (SOP), in which they are postulated to operate in the reverse direction, oxidizing sulfite to APS. Newly developed PCR assays allowed the amplification of 92–93 % (2.1–2.3 kb) of the APS reductase locus . PCR-based screening of 116 taxonomically divergent SOP reference strains revealed a distribution of restricted to photo- and chemotrophs with strict anaerobic or at least facultative anaerobic lifestyles, including , , , and invertebrate symbionts. In the AprBA-based tree, the SOP diverge into two distantly related phylogenetic lineages, Apr lineages I and II, with the proteins of lineage II ( and others) in closer affiliation to the enzymes of the sulfate-reducing prokaryotes (SRP). This clustering is discordant with the dissimilatory sulfite reductase (DsrAB) phylogeny and indicates putative lateral gene transfer from SRP to the respective SOB lineages. In support of lateral gene transfer (LGT), several beta- and gammaproteobacterial species harbour both homologues, the DsrAB-congruent ‘authentic’ and the SRP-related, LGT-derived gene loci, while some relatives possess exclusively the SRP-related genes as a possible result of resident gene displacement by the xenologue. The two-gene state might be an intermediate in the replacement of the resident essential gene. Collected genome data demonstrate the correlation between the AprBA tree topology and the composition/arrangement of the gene loci (occurrence of or genes) from SRP and SOP of lineages I and II. The putative functional role of the SRP-related APS reductases in photo- and chemotrophic SOP is discussed.

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Keyword(s): APAT, adenylylsulfate, phosphate adenylyltransferase , APS, adenosine-5′-phosphosulfate , DG-DGGE, double-gradient DGGE , DGGE, denaturing gradient gel electrophoresis , LGT, lateral gene transfer , SAOR, sulfite, acceptor oxidoreductase , SDR, sulfur dioxygenase , SOB, sulfur-oxidizing bacteria , SOP, sulfur-oxidizing prokaryotes , SQR, sulfide, quinone oxidoreductase and SRP, sulfate-reducing prokaryotes
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2007-10-01
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References

  1. Beller H. R., Chain P. S. G., Letain T. E., Chakicherla A., Larimer F. W., Richardson P. M., Coleman M. A., Wood A. P., Kelly D. P. 2006; The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans . J Bacteriol 188:1473–1488
     [Google Scholar]
  2. Bergin C., Berwig N., Blazejak A., Rühland C., Dubilier N. 2006 Novel Symbiont in the Gutless Marine Oligochaete Inanidrilus exumae . Poster no. P037 presented at the International Symposium on Microbial Sulfur Metabolism (ISMSM) Münster: 29 June to 2 July 2006
    [Google Scholar]
  3. Blazejak A., Kuever J., Erseus C., Amann R., Dubilier N. 2006; Phylogeny of 16S rRNA, ribulose 1,5-bisphosphate carboxylase/oxygenase and adenosine 5′-phosphosulfate reductase genes from gamma- and alphaproteobacterial symbionts in gutless marine worms (Oligochaeta) from Bermuda and the Bahamas. Appl Environ Microbiol 72:5527–5536
     [Google Scholar]
  4. Bright M., Giere O. 2005; Microbial symbiosis in Annelida. Symbiosis 38:1–45
     [Google Scholar]
  5. 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: Springer;
     [Google Scholar]
  6. Brüser T., Lens P. N. L., Trüper H. G. 2000; The biological sulfur cycle. In Environmental Technologies to Treat Sulfur Pollution pp 47–86 Edited by Lens P. N. L., Pol L. H. London: IWA Publishing;
     [Google Scholar]
  7. Cary S. C., Giovannoni S. J. 1993; Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc Natl Acad Sci U S A 90:5695–5699
     [Google Scholar]
  8. Cavanaugh C. M., McKiness Z. P., Newton I. L. G., Stewart F. J. 2001; Marine chemosynthetic symbioses. In The Prokaryotes an Evolving Electronic Resource for the Microbial Community Edited by Dworkin M., Falkow E., Rosenberg E., Schleifer K.-H., Stackebrandt E. New York: Fischer Verlag;
     [Google Scholar]
  9. Dahl C. 1996; Insertional gene inactivation in a phototrophic sulphur bacterium: APS-reductase-deficient mutants of Chromatium vinosum . Microbiology 142:3363–3372
     [Google Scholar]
  10. Dahl C., Trüper H. G., Peck H. Jr 1994; Enzymes of dissimilatory sulfide oxidation in phototrophic sulfur bacteria. In Inorganic Microbial Sulfur Metabolism (Methods in Enzymology vol. 243 pp 400–421 Edited by LeGall J., Abelson J, Simon M. San Diego, CA: Academic Press;
     [Google Scholar]
  11. Dahl C., Rakhely G., Pott-Sperling A. S., Fodor B., Takacs M., Toth A., Kraeling M., Gyorfi K., Kovacs A. other authors 1999; Genes involved in hydrogen and sulfur metabolism in phototrophic sulfur bacteria. FEMS Microbiol Lett 180:317–324
     [Google Scholar]
  12. Dahl C., Engels S., Pott-Sperling A. S., Schulte A., Sander J., Lubbe Y., Deuster O., Brune D. C. 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
     [Google Scholar]
  13. Dubinina G. A., Grabovich M. Y., Chernyshova Y. Y. 2004; The role of oxygen in the regulation of the metabolism of aerotolerant Spirochetes, a major component of “ Thiodendron ” bacterial sulfur mats. Microbiologiia 73:725–733 in Russian
    [Google Scholar]
  14. Ehrenreich A., Widdel F. 1994; Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Appl Environ Microbiol 60:4517–4526
     [Google Scholar]
  15. Friedrich C. G. 1997; Physiology and genetics of sulfur-oxidizing bacteria. In Advances in Microbial Physiology 39 pp 235–289 Edited by Poole R. K. San Diego, CA: Academic Press;
     [Google Scholar]
  16. Friedrich M. W. 2002; Phylogenetic analysis reveals multiple lateral transfers of adenosine-5′-phosphosulfate reductase genes among sulfate-reducing microorganisms. J Bacteriol 184:278–289
     [Google Scholar]
  17. Friedrich C. G., Rother D., Bardischewsky F., Quentmeier A., Fischer J. 2001; Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism?. Appl Environ Microbiol 67:2873–2882
     [Google Scholar]
  18. Fritz G., Buchert T., Huber H., Stetter K. O., Kroneck P. M. H. 2000; Adenylylsulfate reductases from archaea and bacteria are 1: 1 αβ -heterodimeric iron–sulfur flavoenzymes – high similarity of molecular properties emphasizes their central role in sulfur metabolism. FEBS Lett 473:63–66
     [Google Scholar]
  19. Fritz G., Roth A., Schiffer A., Buchert T., Bourenkov G., Bartunik H. D., Huber H., Stetter K. O., Kroneck P. M. H., Ermler U. 2002; Structure of adenylylsulfate reductase from the hyperthermophilic Archaeoglobus fulgidus at 1.6 Å resolution. Proc Natl Acad Sci U S A 99:1836–1841
     [Google Scholar]
  20. Giovannoni S. J., Tripp H. J., Givan S., Podar M., Vergin K. L., Baptista D., Bibbs L., Eads J., Richardson T. H. other authors 2005; Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:1242–1245
     [Google Scholar]
  21. Griesbeck C., Hauska G., Schütz M. 2000; Biological sulfide oxidation: sulfide-quinone reductase (SQR), the primary reaction. In Recent Research Developments in Microbiology 4 pp 179–203 Edited by Pandalai S. G. Trivadrum, India: Research Signpost;
     [Google Scholar]
  22. Haveman S. A., Greene E. A., Stilwell C. P., Voordouw J. K., Voordouw G. 2004; Physiological and gene expression analysis of inhibition of Desulfovibrio vulgaris Hildenborough by nitrite. J Bacteriol 186:7944–7950
     [Google Scholar]
  23. Hipp W. M., Pott A. S., Thum-Schmitz N., Faath I., Dahl C., Trüper H. G. 1997; Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes. Microbiology 143:2891–2902
     [Google Scholar]
  24. Huber H., Prangishvili D. 2000; Sulfolobales . In The Prokaryotes an Evolving Electronic Resource for the Microbial Community Edited by Dworkin M., Falkow E., Rosenberg E., Schleifer K.-H., Stackebrandt E. New York: Fischer Verlag;
     [Google Scholar]
  25. Hurtado L. A., Mateos M., Lutz R. A., Vrijenhoek R. C. 2003; Coupling of bacterial endosymbiont and host mitochondrial genomes in the hydrothermal vent clam Calyptogena magnifica . Appl Environ Microbiol 69:2058–2064
     [Google Scholar]
  26. Imhoff J. F. 2001a; The Chromatiaceae . In The Prokaryotes an Evolving Electronic Resource for the Microbial Community Edited by Dworkin M., Falkow E., Rosenberg E., Schleifer K.-H., Stackebrandt E. New York: Springer Verlag;
     [Google Scholar]
  27. Imhoff J. F. 2001b The phototrophic alpha-Proteobacteria. In The Prokaryotes an Evolving Electronic Resource for the Microbial Community Edited by Dworkin M., Falkow E., Rosenberg E., Schleifer K.-H., Stackebrandt E. New York: Springer Verlag;
     [Google Scholar]
  28. Imhoff J. F. 2003; Phylogenetic taxonomy of the family Chlorobiaceae on the basis of 16S rRNA and fmo (Fenna-Matthews-Olson protein) gene sequences. Int J Syst Evol Microbiol 53:941–951
     [Google Scholar]
  29. Kappler U., Bailey S. 2005; Molecular basis of intramolecular electron transfer in sulfite-oxidizing enzymes is revealed by high resolution structure of a heterodimeric complex of the catalytic molybdopterin subunit and a c -type cytochrome subunit. J Biol Chem 280:24999–25007
     [Google Scholar]
  30. Kappler U., Dahl C. 2001; Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol Lett 203:1–9
     [Google Scholar]
  31. Kelly D. P. 1999; Thermodynamic aspects of energy conservation by chemolithotrophic sulfur bacteria in relation to the sulfur oxidation pathways. Arch Microbiol 171:219–229
     [Google Scholar]
  32. Kelly D. P., Wood A. P. 2000; Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen.nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol 50:511–516
     [Google Scholar]
  33. Klein M., Friedrich M., Roger A. J., Hugenholtz P., Fishbain S., Abicht H., Blackall L. L., Stahl D. A., Wagner M. 2001; Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. J Bacteriol 183:6028–6035
     [Google Scholar]
  34. Kletzin A., Urich T., Muller F., Bandeiras T. M., Gomes C. M. 2004; Dissimilatory oxidation and reduction of elemental sulfur in thermophilic archaea. J Bioenerg Biomembr 36:77–91
     [Google Scholar]
  35. Kuever J., Sievert S. M., Stevens H., Brinkhoff T., Muyzer G. 2002; Microorganisms of the oxidative and reductive part of the sulfur cycle at a shallow-water hydrothermal vent in the Aegean Sea (Milos, Greece. Cah Biol Mar 43:413–416
     [Google Scholar]
  36. Kwok S., Kellogg D. E., McKinney N., Spasic D., Goda L., Levenson C., Sninsky J. J. 1990; Effects of primer-template mismatches on the polymerase chain reaction. Nucleic Acids Res 18:999–1005
     [Google Scholar]
  37. LaRiviere J. W. M., Schmidt K. 2001; Morphologically conspicuous sulfur-oxidizing Eubacteria . In The Prokaryotes an Evolving Electronic Resource for the Microbial Community Edited by Dworkin M., Falkow E., Rosenberg E., Schleifer K.-H., Stackebrandt E. New York: Fischer Verlag;
     [Google Scholar]
  38. Lawrence J. G., Ochman H. 1997; Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol 44:383–397
     [Google Scholar]
  39. Malmstrom R. R., Kiene R. P., Cottrell M. T., Kirchman D. L. 2004; Contribution of SAR11 bacteria to dissolved dimethylsulfoniopropionate and amino acid uptake in the North Atlantic Ocean. Appl Environ Microbiol 70:4129–4135
     [Google Scholar]
  40. Markert S., Arndt C., Felbeck H., Becher D., Sievert S. M., Hügler M., Albrecht D., Robidart J., Bench S., Feldman R. A., Hecker M., Schweder T. 2007; Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila . Science 315:247–250
     [Google Scholar]
  41. Meyer B., Kuever J. 2007; Phylogeny of the alpha and beta subunits of the dissimilatory adenosine-5'-phosphosulfate (APS) reductase from sulfate-reducing prokaryotes – origin and evolution of the dissimilatory sulfate-reduction pathway. Microbiology 153:2026–2044
     [Google Scholar]
  42. Meyer B., Imhoff J. F., 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 in press
    [Google Scholar]
  43. Molin S., Tolker-Nielsen T. 2003; Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14:255–261
     [Google Scholar]
  44. Muyzer G., Teske A., Wirsen C. O., 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
     [Google Scholar]
  45. Nelson D. C., Fisher C. R. 1995; Chemoautotrophic and methanoautotrophic endosymbiontic bacteria at deep-sea vents and seeps. In Microbiology of Deep Sea Hydrothermal Vents pp 125–167 Edited by Karl D. M. Boca Raton, FL: CRC Press;
     [Google Scholar]
  46. Newton I. L. G., 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]
  47. Odintsova E. V., Wood A. P., Kelly D. P. 1993; Chemolithoautotrophic growth of Thiothrix ramosa . Arch Microbiol 160:152–157
     [Google Scholar]
  48. Overmann J., Garcia-Pichel F. 2001; The phototrophic way of life. In The Prokaryotes an Evolving Electronic Resource for the Microbial Community Edited by Dworkin M., Falkow E., Rosenberg E., Schleifer K.-H., Stackebrandt E. New York: Fischer Verlag;
     [Google Scholar]
  49. Peek A. S., Vrijenhoek R. C., Gaut B. S. 1998; Accelerated evolutionary rate in sulfur-oxidizing endosymbiotic bacteria associated with the mode of symbiont transmission. Mol Biol Evol 15:1514–1523
     [Google Scholar]
  50. Pires R. H., Lourenco A. I., Morais F., Teixeira M., Xavier A. V., Saraiva L. M., Pereira I. A. C. 2003; A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774. Bba-Bioenergetics 160567–82
     [Google Scholar]
  51. Pires R. H., Venceslau S. S., Morais F., Teixeira M., Xavier A. V., Pereira I. A. C. 2006; Characterization of the Desulfovibrio desulfuricans ATCC 27774 DsrMKJOP complex – a membrane-bound redox complex involved in the sulfate respiratory pathway. Biochemistry 45:249–262
     [Google Scholar]
  52. Polz M. F., Odintsova E. V., Cavanaugh C. M. 1996; Phylogenetic relationships of the filamentous sulfur bacterium Thiothrix ramosa based on 16S rRNA sequence analysis. Int J Syst Bacteriol 46:94–97
     [Google Scholar]
  53. Pott A. S., 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
     [Google Scholar]
  54. Robertson L. A., Kuenen G. J. 2001; The genus Thiobacillus . In The Prokaryotes An Evolving Electronic Resource for the Microbial Community Edited by Dworkin M., Falkow E., Rosenberg E., Schleifer K.-H., Stackebrandt E. New York: Fischer Verlag;
     [Google Scholar]
  55. Rohwerder T., Sand W. 2003; The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp. Microbiology 149:1699–1710
     [Google Scholar]
  56. Sabehi G., Loy A., Jung K. H., Partha R., Spudich J. L., Isaacson T., Hirschberg J., Wagner M., Beja O. 2005; New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol 3:1409–1417
     [Google Scholar]
  57. Sanchez O., Ferrera I., Dahl C., Mas J. 2001; In vivo role of adenosine-5′-phosphosulfate reductase in the purple sulfur bacterium Allochromatium vinosum . Arch Microbiol 176:301–305
     [Google Scholar]
  58. Sander J., Engels-Schwarzlose S., Dahl C. 2006; Importance of the DsrMKJOP complex for sulfur oxidation in Allochromatium vinosum and phylogenetic analysis of related complexes in other prokaryotes. Arch Microbiol 186:357–366
     [Google Scholar]
  59. Schedel M., Trüper H. G. 1980; Anaerobic oxidation of thiosulfate and elemental sulfur in Thiobacillus denitrificans . Arch Microbiol 124:205–210
     [Google Scholar]
  60. Schiffer A., Fritz G., Kroneck P. M. H., Ermler U. 2006; Reaction mechanism of the iron–sulfur flavoenzyme adenosine-5′-phosphosulfate reductase based on the structural characterization of different enzymatic states. Biochemistry 45:2960–2967
     [Google Scholar]
  61. Simsek M., Adnan H. 2000; Effect of single mismatches at 3′-end of primers on polymerase chain reaction. Med Sci ( Paris ) 2:11–14
     [Google Scholar]
  62. Sorensen S. J., Bailey M., Hansen L. H., Kroer N., Wuertz S. 2005; Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Microbiol 3:700–710
     [Google Scholar]
  63. Suzuki I. 1994; Sulfur-oxidizing enzymes. In Inorganic Microbial Sulfur Metabolism (Methods in Enzymology 243 pp 455–462 San Diego, CA: Academic Press;
     [Google Scholar]
  64. Takai K., Campbell B. J., Cary S. C., Suzuki M., Oida H., Nunoura T., Hirayama H., Nakagawa S., Suzuki Y. other authors 2005; Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria . Appl Environ Microbiol 71:7310–7320
     [Google Scholar]
  65. Taylor B. F. 1994; Adenylylsulfate reductases from thiobacilli. In Inorganic Microbial Sulfur Metabolism (Methods in Enzymology 243 pp 393–400 San Diego, CA: Academic Press;
     [Google Scholar]
  66. Teske A., Nelson D. C. 2004; The genera Beggiatoa and Thioploca . In The Prokaryotes An Evolving Electronic Resource for the Microbial Community Edited by Dworkin M., Falkow E., Rosenberg E., Schleifer K.-H., Stackebrandt E. New York: Springer Verlag;
     [Google Scholar]
  67. 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]
  68. Tonolla M., Peduzzi S., Demarta A., Peduzzi R., Hahn D. 2004; Phototrophic sulfur and sulfate-reducing bacteria in the chemocline of meromictic Lake Cadagno, Switzerland. Journal of Limnology 63:161–170
     [Google Scholar]
  69. Trüper H. G., Fischer U. 1982; Anaerobic oxidation of sulfur-compounds as electron-donors for bacterial photosynthesis. Philos Trans R Soc Lon B Biol Sci 298:529–542
     [Google Scholar]
  70. Venter J. C., Remington K., Heidelberg J. F., Halpern A. L., Rusch D., Eisen J. A., Wu D. Y., Paulsen I., Nelson K. E. other authors 2004; Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74
     [Google Scholar]
  71. Visscher P. T., Prins R. A., van Gemerden H. 1992; Rates of sulfate reduction and thiosulfate consumption in a marine microbial mat. FEMS Microbiol Ecol 86:283–294
     [Google Scholar]
  72. Woyke T., Teeling H., Ivanova N. N., Huntemann M., Richter M., Gloeckner F. O., Boffelli D., Anderson I. J., Barry K. W. other authors 2006; Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443:950–955
     [Google Scholar]
  73. Zimmermann P., Laska S., Kletzin A. 1999; Two modes of sulfite oxidation in the extremely thermophilic and acidophilic archaeon Acidianus ambivalens . Arch Microbiol 172:76–82
     [Google Scholar]
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Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5′-phosphosulfate reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes
Microbiology 153, 3478 (2007); https://doi.org/10.1099/mic.0.2007/008250-0
/content/journal/micro/10.1099/mic.0.2007/008250-0
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