1887

Abstract

A psychro- and aerotolerant bacterium was isolated from the sulfidic water of a pelagic redox zone of the central Baltic Sea. The slightly curved rod- or spiral-shaped cells were motile by one polar flagellum or two bipolar flagella. Growth was chemolithoautotrophic, with nitrate or nitrite as electron acceptor and either a variety of sulfur species of different oxidation states or hydrogen as electron donor. Although the bacterium was able to utilize organic substances such as acetate, pyruvate, peptone and yeast extract for growth, these compounds yielded considerably lower cell numbers than obtained with reduced sulfur or hydrogen; in addition, bicarbonate supplementation was necessary. The cells also had an absolute requirement for NaCl. Optimal growth occurred at 15 °C and at pH 6.6–8.0. The predominant fatty acid of this organism was 16 : 1ω7, with 3-OH 14 : 0, 16 : 0, 16 : 1ω5+ and 18 : 1ω7 present in smaller amounts. The DNA G+C content was 33.6 mol%. As determined in 16S rRNA gene sequence phylogeny analysis, the isolate belongs to the genus , within the class , with 93.7 to 94.2 % similarity to the other species of the genus , , and . However, the distinct physiological and genotypic differences from these previously described taxa support the description of a novel species, sp. nov. The type strain is GD1 ( = DSM 19862 = JCM 16533). Our results also justify an emended description of the genus .

Funding
This study was supported by the:
  • Deutsche Forschungsgemeinschaft (Award LA 1466/4-2 and LA 1466/4-1)
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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2013-11-01
2024-10-12
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References

  1. Alonso-Sáez L., Galand P. E., Casamayor E. O., Pedrós-Alió C., Bertilsson S. ( 2010 ). High bicarbonate assimilation in the dark by Arctic bacteria. . ISME J 4, 15811590. [View Article] [PubMed]
    [Google Scholar]
  2. Balch W. E., Fox G. E., Magrum L. J., Woese C. R., Wolfe R. S. ( 1979 ). Methanogens: reevaluation of a unique biological group. . Microbiol Rev 43, 260296.[PubMed]
    [Google Scholar]
  3. Boschker H. T. S. ( 2004 ). Linking microbial community structure and functioning: stable isotope (13C) labeling in combination with PLFA analysis. . In Molecular Microbial Ecology Manual II, pp. 16731688. Edited by Kowalchuk G. A., de Bruijn F. J., Head I. M., Akkermans A. D., van Elsas J. D. . Dordrecht:: Kluwer Academic Publishers;.
    [Google Scholar]
  4. Brettar I., Rheinheimer G. ( 1991 ). Denitrification in the central Baltic: evidence for H2S-oxidation as motor of denitrification at the oxic-anoxic interface. . Mar Ecol Prog Ser 77, 157169. [View Article]
    [Google Scholar]
  5. Brettar I., Labrenz M., Flavier S., Bötel J., Kuosa H., Christen R., Höfle 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, 13641372. [View Article] [PubMed]
    [Google Scholar]
  6. Brinkhoff T., Kuever J., Muyzer G., Jannasch H. W. ( 2005 ). Genus VI. Thiomicrospira. . In Bergey’s Manual of Systematic Bacteriology, , 2nd edn., vol. 2, part B, pp. 193199. Edited by Brenner D. J., Krieg N. R., Staley J. T. . New York:: Springer;.
    [Google Scholar]
  7. Bruns A., Cypionka H., Overmann J. ( 2002 ). Cyclic AMP and acyl homoserine lactones increase the cultivation efficiency of heterotrophic bacteria from the central Baltic Sea. . Appl Environ Microbiol 68, 39783987. [View Article] [PubMed]
    [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, 458468. [View Article] [PubMed]
    [Google Scholar]
  9. Dehority B. A. ( 1971 ). Carbon dioxide requirement of various species of rumen bacteria. . J Bacteriol 105, 7076.[PubMed]
    [Google Scholar]
  10. Engel A. S., Porter M. L., Stern L. A., Quinlan S., Bennett P. C. ( 2004 ). Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic “Epsilonproteobacteria”. . FEMS Microbiol Ecol 51, 3153. [View Article] [PubMed]
    [Google Scholar]
  11. Glaubitz S., Lueders T., Abraham W.-R., Jost G., Jürgens K., Labrenz M. ( 2009 ). 13C-isotope analyses reveal that chemolithoautotrophic Gamma- and Epsilonproteobacteria feed a microbial food web in a pelagic redoxcline of the central Baltic Sea. . Environ Microbiol 11, 326337. [View Article] [PubMed]
    [Google Scholar]
  12. Glaubitz S., Labrenz M., Jost G., Jürgens K. ( 2010 ). Diversity of active chemolithoautotrophic prokaryotes in the sulfidic zone of a Black Sea pelagic redoxcline as determined by rRNA-based stable isotope probing. . FEMS Microbiol Ecol 74, 3241. [View Article] [PubMed]
    [Google Scholar]
  13. Grote J., Labrenz M., Pfeiffer B., Jost G., Jürgens K. ( 2007 ). Quantitative distributions of Epsilonproteobacteria and a Sulfurimonas subgroup in pelagic redoxclines of the central Baltic Sea. . Appl Environ Microbiol 73, 71557161. [View Article] [PubMed]
    [Google Scholar]
  14. Grote J., Jost G., Labrenz M., Herndl G. J., Jürgens K. ( 2008 ). Epsilonproteobacteria represent the major portion of chemoautotrophic bacteria in sulfidic waters of pelagic redoxclines of the Baltic and Black Seas. . Appl Environ Microbiol 74, 75467551. [View Article] [PubMed]
    [Google Scholar]
  15. Grote J., Schott T., Bruckner C. G., Glöckner F. O., Jost G., Teeling H., Labrenz M., Jürgens K. ( 2012 ). Genome and physiology of a model Epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones. . Proc Natl Acad Sci U S A 109, 506510. [View Article] [PubMed]
    [Google Scholar]
  16. Hannig M., Lavik G., Kuypers M. M. M., Woebken D., Martens-Habbena W., Jürgens K. ( 2007 ). Shift from denitrification to anammox after inflow events in the central Baltic Sea. . Limnol Oceanogr 52, 13361345. [View Article]
    [Google Scholar]
  17. Inagaki F., Takai K., Kobayashi H., Nealson K. H., Horikoshi K. ( 2003 ). Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing ϵ-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. . Int J Syst Evol Microbiol 53, 18011805. [View Article] [PubMed]
    [Google Scholar]
  18. Jensen M. M., Petersen J., Dalsgaard T., Thamdrup B. ( 2009 ). Pathways, rates, and regulation of N2 production in the chemocline of an anoxic basin, Mariager Fjord, Denmark. . Mar Chem 113, 102113. [View Article]
    [Google Scholar]
  19. Jost G., Zubkov M. V., Yakushev E., Labrenz M., Jürgens K. ( 2008 ). High abundance and dark CO2 fixation of chemolithoautotrophic prokaryotes in anoxic waters of the Baltic Sea. . Limnol Oceanogr 53, 1422. [View Article]
    [Google Scholar]
  20. Jost G., Martens-Habbena W., Pollehne F., Schnetger B., Labrenz M. ( 2010 ). Anaerobic sulfur oxidation in the absence of nitrate dominates microbial chemoautotrophy beneath the pelagic chemocline of the eastern Gotland Basin, Baltic Sea. . FEMS Microbiol Ecol 71, 226236. [View Article] [PubMed]
    [Google Scholar]
  21. Labrenz M., Brettar I., Christen R., Flavier S., Bötel J., Höfle M. G. ( 2004 ). Development and application of a real-time PCR approach for quantification of uncultured bacteria in the central Baltic Sea. . Appl Environ Microbiol 70, 49714979. [View Article] [PubMed]
    [Google Scholar]
  22. Labrenz M., Jost G., Pohl C., Beckmann S., Martens-Habbena W., Jürgens K. ( 2005 ). Impact of different in vitro electron donor/acceptor conditions on potential chemolithoautotrophic communities from marine pelagic redoxclines. . Appl Environ Microbiol 71, 66646672. [View Article] [PubMed]
    [Google Scholar]
  23. Labrenz M., Jost G., Jürgens K. ( 2007 ). Distribution of abundant prokaryotic organisms in the water column of the central Baltic Sea with an oxic-anoxic interface. . Aquat Microb Ecol 46, 177190. [View Article]
    [Google Scholar]
  24. Lepland A., Stevens R. L. ( 1998 ). Manganese authigenesis in the Landsort Deep, Baltic Sea. . Mar Geol 151, 125. [View Article]
    [Google Scholar]
  25. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar, Buchner A., Lai T., Steppi S. & other authors ( 2004 ). arb: a software environment for sequence data. . Nucleic Acids Res 32, 13631371. [View Article] [PubMed]
    [Google Scholar]
  26. Nakagawa S., Takai K. ( 2008 ). Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. . FEMS Microbiol Ecol 65, 114. [View Article] [PubMed]
    [Google Scholar]
  27. Nakagawa S., Takai K., Inagaki F., Hirayama H., Nunoura T., Horikoshi K., Sako Y. ( 2005 ). Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. . Environ Microbiol 7, 16191632. [View Article] [PubMed]
    [Google Scholar]
  28. Neretin L. N., Pohl C., Jost G., Leipe T., Pollehne F. ( 2003 ). Manganese cycling in the Gotland Deep, Baltic Sea. . Mar Chem 82, 125143. [View Article]
    [Google Scholar]
  29. Pearson W. R., Lipman D. J. ( 1988 ). Improved tools for biological sequence comparison. . Proc Natl Acad Sci U S A 85, 24442448. [View Article] [PubMed]
    [Google Scholar]
  30. Sasser M. ( 1990 ). Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Technical Note 101. Newark, DE:: Microbial ID;.
    [Google Scholar]
  31. Sievert S. M., Scott K. M., Klotz M. G., Chain P. S., Hauser L. J., Hemp J., Hügler M., Land M., Lapidus A. & other authors ( 2008 ). Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans . . Appl Environ Microbiol 74, 11451156. [View Article] [PubMed]
    [Google Scholar]
  32. Stackebrandt E., Goebel B. M. ( 1994 ). Taxonomic Note: A place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in Bacteriology. . Int J Syst Bacteriol 44, 846849. [View Article]
    [Google Scholar]
  33. Starkenburg S. R., Arp D. J., Bottomley P. J. ( 2008 ). d-Lactate metabolism and the obligate requirement for CO2 during growth on nitrite by the facultative lithoautotroph Nitrobacter hamburgensis . . Microbiology 154, 24732481. [View Article] [PubMed]
    [Google Scholar]
  34. Suzuki Y., Sasaki T., Suzuki M., Nogi Y., Miwa T., Takai K., Nealson K. H., Horikoshi K. ( 2005 ). Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. . Appl Environ Microbiol 71, 54405450. [View Article] [PubMed]
    [Google Scholar]
  35. Suzuki Y., Kojima S., Sasaki T., Suzuki M., Utsumi T., Watanabe H., Urakawa H., Tsuchida S., Nunoura T. & other authors ( 2006 ). Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. . Appl Environ Microbiol 72, 13881393. [View Article] [PubMed]
    [Google Scholar]
  36. Takai K., Suzuki M., Nakagawa S., Miyazaki M., Suzuki Y., Inagaki F., Horikoshi K. ( 2006 ). Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas . . Int J Syst Evol Microbiol 56, 17251733. [View Article] [PubMed]
    [Google Scholar]
  37. Timmer-ten Hoor A. ( 1975 ). A new type of thiosulphate oxidizing, nitrate reducing microorganism: Thiomicrospira denitrificans sp. nov.. . Neth J Sea Res 9, 344350. [View Article]
    [Google Scholar]
  38. Widdel F., Bak F. ( 1992 ). Chapter 183. Gram-negative mesophilic sulfate-reducing bacteria. . In The Prokaryotes. , 2nd edn., vol. IV, pp, 33523378. Edited by Balows A., Trüper H. G., Dworkin M., Harder W., Schleifer K.-H. . New York:: Springer;. [CrossRef]
    [Google Scholar]
  39. Widdel F., Kohring G. W., Mayer F. ( 1983 ). Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. III. Characterization of the filamentous gliding Desulfonema limicola gen. nov. sp. nov., and Desulfonema magnum sp. nov.. Arch Microbiol 134, 286294. [View Article]
    [Google Scholar]
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