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Volume 63, Issue Pt_11

gen. nov., sp. nov., belonging to the globally distributed RCA cluster of the marine clade, isolated from the German Wadden Sea Free

Abstract

Four heterotrophic bacterial strains belonging to the globally distributed marine RCA ( clade-affiliated) cluster (family , class ) were obtained from coastal seawater samples. Strain RCA23 was isolated from a 10 dilution culture inoculated with seawater from the German Wadden Sea (southern North Sea), reflecting the high abundance of RCA bacteria in this habitat. Strains IMCC1909, IMCC1923 and IMCC1933 were isolated from diluted seawater (10) of the Yellow Sea, South Korea. Based on 16S rRNA gene sequence comparison, 307 is the closest described relative of the RCA strains, with 95.4–95.5 % sequence similarity. Cells of RCA23, IMCC1909, IMCC1923 and IMCC1933 are small motile rods requiring sodium ions. Optimal growth of RCA23 occurs at 25 °C and within a very narrow pH range (pH 7–8, optimum pH 7.5). The DNA G+C base content of RCA23 is 53.67 mol%. The major respiratory lipoquinone is ubiquinone-10 (Q-10) and the dominant fatty acids (>1 %) are 12 : 1 3-OH, 16 : 1ω7, 16 : 0, 18 : 1ω7, 18 : 0 and 11-methyl 18 : 1ω7. The polar lipid pattern indicated the presence of phosphatidylglycerol, two unidentified aminolipids and two unidentified phospholipids. On marine agar, RCA23 forms non-pigmented, transparent to light beige, small (<1 mm), circular, convex colonies. Strain RCA23 harbours all genes for the production of bacteriochlorophyll (BChl ). Genes encoding the light-harvesting reaction centre of BChl () were identified in all RCA strains. No visible pigmentation was observed for any of the strains under laboratory conditions, but spectrophotometric analysis revealed weak production of BChl by RCA23. Morphological, physiological and genotypic features of strain RCA23 suggest that it represents a novel species of a new genus within the , for which we propose the name gen. nov., sp. nov., described previously by Giebel [ (2011), 8–19] as ‘ Planktomarina temperata’. The type strain of is RCA23 ( = DSM 22400 = JCM 18269).

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Funding
This study was supported by the:
  • Deutsche Forschungsgemeinschaft (DFG)
  • Special Priority Program on Antarctic Research
  • Transregional Collaborative Research Center (Award TRR-51)
  • 21C Frontier Program of Microbial Genomics and Applications funded by MEST, Republic of Korea
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2013-11-01
2024-04-24
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References

  1. Allgaier M., Uphoff H., Felske A., Wagner-Döbler I. ( 2003 ). Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats. . Appl Environ Microbiol 69, 5051–5059. [View Article] [PubMed]
    [Google Scholar]
  2. Arahal D. R., Macián M. C., Garay E., Pujalte M. J. ( 2005 ). Thalassobius mediterraneus gen. nov., sp. nov., and reclassification of Ruegeria gelatinovorans as Thalassobius gelatinovorus comb. nov.. Int J Syst Evol Microbiol 55, 2371–2376. [View Article] [PubMed]
    [Google Scholar]
  3. Brinkhoff T., Muyzer G. ( 1997 ). Increased species diversity and extended habitat range of sulfur-oxidizing Thiomicrospira spp.. Appl Environ Microbiol 63, 3789–3796.[PubMed]
    [Google Scholar]
  4. Brinkhoff T., Giebel H.-A., Simon M. ( 2008 ). Diversity, ecology, and genomics of the Roseobacter clade: a short overview. . Arch Microbiol 189, 531–539. [View Article] [PubMed]
    [Google Scholar]
  5. Buchan A., González J. M., Moran M. A. ( 2005 ). Overview of the marine Roseobacter lineage. . Appl Environ Microbiol 71, 5665–5677. [View Article] [PubMed]
    [Google Scholar]
  6. Chávez F. P., Lünsdorf H., Jerez C. A. ( 2004 ). Growth of polychlorinated-biphenyl-degrading bacteria in the presence of biphenyl and chlorobiphenyls generates oxidative stress and massive accumulation of inorganic polyphosphate. . Appl Environ Microbiol 70, 3064–3072. [View Article] [PubMed]
    [Google Scholar]
  7. Cho J.-C., Giovannoni S. J. ( 2004 ). Oceanicola granulosus gen. nov., sp. nov. and Oceanicola batsensis sp. nov., poly-β-hydroxybutyrate-producing marine bacteria in the order ‘Rhodobacterales’. . Int J Syst Evol Microbiol 54, 1129–1136. [View Article] [PubMed]
    [Google Scholar]
  8. Clayton R. K. ( 1966 ). Spectroscopic analysis of bacteriochlorophylls in vitro and in vivo . . Photochem Photobiol 5, 669–677. [View Article]
    [Google Scholar]
  9. Connon S. A., Giovannoni S. J. ( 2002 ). High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. . Appl Environ Microbiol 68, 3878–3885. [View Article] [PubMed]
    [Google Scholar]
  10. Garrity G. M., Bell J. A., Lilburn T. ( 2006 ). Order III. Rhodobacterales ord. nov. In List of New Names and New Combinations Previously Effectively, but not Validly, Published, Validation list no. 107. . Int J Syst Evol Microbiol 56, 1–6. [View Article] [PubMed]
    [Google Scholar]
  11. Giebel H.-A., Brinkhoff T., Zwisler W., Selje N., Simon M. ( 2009 ). Distribution of Roseobacter RCA and SAR11 lineages and distinct bacterial communities from the subtropics to the Southern Ocean. . Environ Microbiol 11, 2164–2178. [View Article] [PubMed]
    [Google Scholar]
  12. Giebel H.-A., Kalhoefer D., Lemke A., Thole S., Gahl-Janssen R., Simon M., Brinkhoff T. ( 2011 ). Distribution of Roseobacter RCA and SAR11 lineages in the North Sea and characteristics of an abundant RCA isolate. . ISME J 5, 8–19. [View Article] [PubMed]
    [Google Scholar]
  13. Gosink J. J., Herwig R. P., Staley J. T. ( 1997 ). Octadecabacter arcticus gen. nov., sp. nov., and O. antarcticus, sp. nov., nonpigmented, psychrophilic gas vacuolate bacteria from polar sea ice and water. . Int J Syst Bacteriol 20, 356–365.
     [Google Scholar]
  14. Gregersen T. ( 1978 ). Rapid method for distinction of Gram-negative from Gram-positive Bacteria. . Appl Microbiol Biotechnol 5, 123–127. [View Article]
    [Google Scholar]
  15. Hahnke S., Tindall B. J., Schumann P., Sperling M., Brinkhoff T., Simon M. ( 2012 ). Planktotalea frisia gen. nov., sp. nov., isolated from the southern North Sea. . Int J Syst Evol Microbiol 62, 1619–1624. [View Article] [PubMed]
    [Google Scholar]
  16. Hoppe H. G. ( 1993 ). Use of fluorogenic model substrates for extracellular enzyme activity (EEA) measurement of bacteria. . In Handbook of Methods in Aquatic Microbial Ecology, pp. 423–431. Edited by Kemp P. F., Sherr B. F., Sherr E. B., Cole J. J. . Boca Raton, FL:: Lewis;.
     [Google Scholar]
  17. Hunt D. E., Klepac-Ceraj V., Acinas S. G., Gautier C., Bertilsson S., Polz M. F. ( 2006 ). Evaluation of 23S rRNA PCR primers for use in phylogenetic studies of bacterial diversity. . Appl Environ Microbiol 72, 2221–2225. [View Article] [PubMed]
    [Google Scholar]
  18. Ivanova E. P., Gorshkova N. M., Sawabe T., Zhukova N. V., Hayashi K., Kurilenko V. V., Alexeeva Y., Buljan V., Nicolau D. V. & other authors ( 2004 ). Sulfitobacter delicatus sp. nov. and Sulfitobacter dubius sp. nov., respectively from a starfish (Stellaster equestris) and sea grass (Zostera marina). . Int J Syst Evol Microbiol 54, 475–480. [View Article] [PubMed]
    [Google Scholar]
  19. Kalhoefer D., Thole S., Voget S., Lehmann R., Liesegang H., Wollher A., Daniel R., Simon M., Brinkhoff T. ( 2011 ). Comparative genome analysis and genome-guided physiological analysis of Roseobacter litoralis . . BMC Genomics 12, 324. [View Article] [PubMed]
    [Google Scholar]
  20. Kang I., Oh H.-M., Vergin K. L., Giovannoni S. J., Cho J. C. ( 2010 ). Genome sequence of the marine alphaproteobacterium HTCC2150, assigned to the Roseobacter clade. . J Bacteriol 192, 6315–6316. [View Article] [PubMed]
    [Google Scholar]
  21. Labrenz M., Collins M. D., Lawson P. A., Tindall B. J., Braker G., Hirsch P. ( 1998 ). Antarctobacter heliothermus gen. nov., sp. nov., a budding bacterium from hypersaline and heliothermal Ekho Lake. . Int J Syst Bacteriol 48, 1363–1372. [View Article] [PubMed]
    [Google Scholar]
  22. Lane D. J. ( 1991 ). 16S/23S rRNA sequencing. . In Nucleic Acid Technology in Bacterial Systematics, pp. 115–175. Edited by Stackebrandt E., Goodfellow M. . New York:: Wiley;.
     [Google Scholar]
  23. Lü L.-G., Liu J., Yu F., Wu W., Yang X. ( 2007 ). Vertical migration of sound scatters in the southern Yellow Sea in summer. . Ocean Sci J 42, 1–8. [View Article]
    [Google Scholar]
  24. 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, 1363–1371. [View Article] [PubMed]
    [Google Scholar]
  25. Lunau M., Lemke A., Walther K., Martens-Habbena W., Simon M. ( 2005 ). An improved method for counting bacteria from sediments and turbid environments by epifluorescence microscopy. . Environ Microbiol 7, 961–968. [View Article] [PubMed]
    [Google Scholar]
  26. Lunau M., Lemke A., Dellwig O., Simon M. ( 2006 ). Physical and biogeochemical controls of microaggregate dynamics in a tidally affected coastal ecosystem. . Limnol Oceanogr 51, 847–859. [View Article]
    [Google Scholar]
  27. Malmstrom R. R., Straza T. R. A., Cottrell M. T., Kirchman D. L. ( 2007 ). Diversity, abundance, and biomass production of bacterial groups in the western Arctic Ocean. . Aquat Microb Ecol 47, 45–55. [View Article]
    [Google Scholar]
  28. Martens T., Heidorn T., Pukall R., Simon M., Tindall B. J., Brinkhoff T. ( 2006 ). Reclassification of Roseobacter gallaeciensis Ruiz-Ponte et al. 1998 as Phaeobacter gallaeciensis gen. nov., comb. nov., description of Phaeobacter inhibens sp. nov., reclassification of Ruegeria algicola (Lafay et al. 1995) Uchino et al. 1999 as Marinovum algicola gen. nov., comb. nov., and emended descriptions of the genera Roseobacter, Ruegeria and Leisingera . . Int J Syst Evol Microbiol 56, 1293–1304. [View Article] [PubMed]
    [Google Scholar]
  29. Mayali X., Franks P. J. S., Azam F. ( 2008 ). Cultivation and ecosystem role of a marine Roseobacter clade-affiliated cluster bacterium. . Appl Environ Microbiol 74, 2595–2603. [View Article] [PubMed]
    [Google Scholar]
  30. Mopper K., Schultz C. A., Chevolot L., Germain C., Revuelta R., Dawson R. ( 1992 ). Determinations of sugars in unconcentrated seawater and other natural waters by liquid chromatography and pulsed ampereometric detection. . Environ Sci Technol 26, 133–138. [View Article]
    [Google Scholar]
  31. Murray R. G. E., Doetsch R. N., Robinow C. F. ( 1994 ). Determinative and cytological light microscopy. . In Methods for General and Molecular Bacteriology, pp. 21–41. Edited by Gerhardt P., Murray R. G. E., Wood W. A., Krieg N. R. . Washington, DC:: American Society for Microbiology;.
     [Google Scholar]
  32. Muyzer G., de Waal E. C., Uitterlinden A. G. ( 1993 ). Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. . Appl Environ Microbiol 59, 695–700.[PubMed]
    [Google Scholar]
  33. Muyzer G., Brinkhoff T., Nübel U., Santegoeds C., Schäfer H., Wawer C. ( 1998 ). Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. . In Molecular Microbial Ecology Manual, pp. 1–27. Edited Akkermans A., de Bruijn F., van Elsas D. . Dordrecht:: Kluwer;.
     [Google Scholar]
  34. Newton R. J., Griffin L. E., Bowles K. M., Meile C., Gifford S., Givens C. E., Howard E. C., King E., Oakley C. A. & other authors ( 2010 ). Genome characteristics of a generalist marine bacterial lineage. . ISME J 4, 784–798. [View Article] [PubMed]
    [Google Scholar]
  35. Otto L., Zimmerman J. T. E., Furnes G. K., Mork M., Saetre R., Becker G. ( 1990 ). Review of the physical oceanography of the North Sea. . Neth J Sea Res 26, 161–238. [View Article]
    [Google Scholar]
  36. Rusch D. B., Halpern A. L., Sutton G., Heidelberg K. B., Williamson S., Yooseph S., Wu D., Eisen J. A., Hoffman J. M. & other authors ( 2007 ). The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. . PLoS Biol 5, e77. [View Article] [PubMed]
    [Google Scholar]
  37. Schaefer J. K., Goodwin K. D., McDonald I. R., Murrell J. C., Oremland R. S. ( 2002 ). Leisingera methylohalidivorans gen. nov., sp. nov., a marine methylotroph that grows on methyl bromide. . Int J Syst Evol Microbiol 52, 851–859. [View Article] [PubMed]
    [Google Scholar]
  38. Schut F., de Vries E. J., Gottschal J. C., Robertson B. R., Harder W., Prins R. A., Button D. K. ( 1993 ). Isolation of typical marine bacteria by dilution culture – growth, maintenance, and characteristics of isolates under laboratory conditions. . Appl Environ Microbiol 59, 2150–2160.[PubMed]
    [Google Scholar]
  39. Selje N., Simon M. ( 2003 ). Composition and dynamics of particle-associated and free-living bacterial communities in the Weser estuary, Germany. . Aquat Microb Ecol 30, 221–237. [View Article]
    [Google Scholar]
  40. Selje N., Simon M., Brinkhoff T. ( 2004 ). A newly discovered Roseobacter cluster in temperate and polar oceans. . Nature 427, 445–448. [View Article] [PubMed]
    [Google Scholar]
  41. Selje N., Brinkhoff T., Simon M. ( 2005 ). Detection of abundant bacteria in the Weser estuary using culture-dependent and culture-independent approaches. . Aquat Microb Ecol 39, 17–34. [View Article]
    [Google Scholar]
  42. Shiba T. ( 1991 ). Roseobacter litoralis gen. nov., sp. nov., and Roseobacter denitrificans sp. nov., aerobic pink-pigmented bacteria which contain bacteriochlorophyll a . . Syst Appl Microbiol 14, 140–145. [View Article]
    [Google Scholar]
  43. Smibert R. M., Krieg N. R. ( 1994 ). Phenotypic characterization. . In Methods for General and Molecular Bacteriology, pp. 607–654. Edited by Gerhardt P., Murray R. G. E., Wood W. A., Krieg N. R. . Washington, DC:: American Society for Microbiology;.
     [Google Scholar]
  44. Sorokin D. Y. ( 1995 ). Sulfitobacter pontiacus gen. nov., sp. nov. – a new heterotrophic bacterium from the Black Sea, specialized on sulfite oxidation. . Microbiology (English translation of Mikrobiologiia) 64, 295–305.
     [Google Scholar]
  45. Stevens H., Brinkhoff T., Simon M. ( 2005 ). Composition of free-living, aggregate-associated and sediment surface-associated bacterial communities in the German Wadden Sea. . Aquat Microb Ecol 38, 15–30. [View Article]
    [Google Scholar]
  46. Strömpl C., Tindall B. J., Jarvis G. N., Lünsdorf N., Moore E. R. B., Hippe H. ( 1999 ). A re-evaluation of the taxonomy of the genus Anaerovibrio, with the reclassification of Anaerovibrio glycerini as Anaerosinus glycerini gen. nov., comb. nov., and Anaerovibrio burkinabensis as Anaeroarcus burkinensis [corrig.] gen. nov., comb. nov.. Int J Syst Bacteriol 49, 1861–1872. [View Article] [PubMed]
    [Google Scholar]
  47. Teske A., Brinkhoff T., Muyzer G., Moser D. P., Rethmeier J., Jannasch H. W. ( 2000 ). Diversity of thiosulfate-oxidizing bacteria from marine sediments and hydrothermal vents. . Appl Environ Microbiol 66, 3125–3133. [View Article] [PubMed]
    [Google Scholar]
  48. Tindall B. J. ( 1990a ). A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. . Syst Appl Microbiol 13, 128–130. [View Article]
    [Google Scholar]
  49. Tindall B. J. ( 1990b ). Lipid composition of Halobacterium lacusprofundi . . FEMS Microbiol Lett 66, 199–202. [View Article]
    [Google Scholar]
  50. Tindall B. J. ( 1996 ). Respiratory lipoquinones as biomarkers. . In Molecular Microbial Ecology Manual, section 4.1.5, supplement 1. Edited by Akkermans A., de Bruijn F., van Elsas D. . Dordrecht:: Kluwer;.
     [Google Scholar]
  51. Wagner-Döbler I., Biebl H. ( 2006 ). Environmental biology of the marine Roseobacter lineage. . Annu Rev Microbiol 60, 255–280. [View Article] [PubMed]
    [Google Scholar]
  52. Wagner-Döbler I., Rheims H., Felske A., Pukall R., Tindall B. J. ( 2003 ). Jannaschia helgolandensis gen. nov., sp. nov., a novel abundant member of the marine Roseobacter clade from the North Sea. . Int J Syst Evol Microbiol 53, 731–738. [View Article] [PubMed]
    [Google Scholar]
  53. Wagner-Döbler I., Rheims H., Felske A., El-Ghezal A., Flade-Schröder D., Laatsch H., Lang S., Pukall R., Tindall B. J. ( 2004 ). Oceanibulbus indolifex gen. nov., sp. nov., a North Sea alphaproteobacterium that produces bioactive metabolites. . Int J Syst Evol Microbiol 54, 1177–1184. [View Article] [PubMed]
    [Google Scholar]
  54. West N. J., Obernosterer I., Zemb O., Lebaron P. ( 2008 ). Major differences of bacterial diversity and activity inside and outside of a natural iron-fertilized phytoplankton bloom in the Southern Ocean. . Environ Microbiol 10, 738–756. [View Article] [PubMed]
    [Google Scholar]
  55. Yoon J. H., Kang S.-J., Oh T.-K. ( 2007 ). Sulfitobacter marinus sp. nov., isolated from seawater of the East Sea in Korea. . Int J Syst Evol Microbiol 57, 302–305. [View Article] [PubMed]
    [Google Scholar]
  56. Yutin N., Suzuki M. T., Béjà O. ( 2005 ). Novel primers reveal wider diversity among marine aerobic anoxygenic phototrophs. . Appl Environ Microbiol 71, 8958–8962. [View Article] [PubMed]
    [Google Scholar]
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Planktomarina temperata gen. nov., sp. nov., belonging to the globally distributed RCA cluster of the marine Roseobacter clade, isolated from the German Wadden Sea
Int J Syst Evol Microbiol 63, 4207 (2013); https://doi.org/10.1099/ijs.0.053249-0
/content/journal/ijsem/10.1099/ijs.0.053249-0
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