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Abstract

A new heterotrophic, aerobic alphaproteobacterium, designated strain SH36 (=DSM 23330=LMG 25292), was obtained from a seawater sample collected in the open North Sea during a phytoplankton bloom. Analysis of the 16S rRNA gene sequence revealed affiliation of strain SH36 to the species (family ), showing 100 and 99.9 % sequence similarity to the 16S rRNA genes of the strains ZXM098 and ZXM100. Digital DNA–DNA hybridization of strain SH36 with the type strain of showed 98.0 % relatedness, confirming that strain SH36 can be classified within the same species. All three strains were compared by physiological, morphological, chemotaxonomic, and genotypic characteristics. The strains showed only minor differences in the composition of fatty acids and polar lipids, but considerable physiological differences. Comparison of the 16S rRNA gene sequence of SH36 with sequences present in GenBank revealed that phylotypes with ≥98.65 % sequence identity to the type strain of were found at different marine and estuarine locations of temperate and subtropic regions. Furthermore, by using a specific PCR approach was detected throughout annual cycles at the offshore station at Helgoland Roads in the German Bight, indicating that this species is a permanent member of the microbial community in the North Sea.

Funding
This study was supported by the:
  • Deutsche Forschungsgemeinschaft
    • Principle Award Recipient: CristinaMoraru
  • Deutsche Forschungsgemeinschaft
    • Principle Award Recipient: ThorstenBrinkhoff
  • Deutsche Forschungsgemeinschaft
    • Principle Award Recipient: MeinhardSimon
  • Volkswagen Foundation
    • Principle Award Recipient: ThorstenBrinkhoff
  • Volkswagen Foundation
    • Principle Award Recipient: MeinhardSimon
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/content/journal/ijsem/10.1099/ijsem.0.006472
2024-07-26
2025-07-12
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References

  1. Li Z, Qu Z, Zhang X. Lentibacter algarum gen. nov., sp. nov., isolated from coastal water during a massive green algae bloom. Int J Syst Evol Microbiol 2012; 62:1042–1047 [View Article]
    [Google Scholar]
  2. Liang KYH, Orata FD, Boucher YF, Case RJ. Roseobacters in a sea of poly- and paraphyly: whole genome-based taxonomy of the family Rhodobacteraceae and the proposal for the split of the “Roseobacter Clade” into a novel family, Roseobacteraceae fam. nov. Front Microbiol 2021; 12:683109 [View Article] [PubMed]
    [Google Scholar]
  3. Buchan A, González JM, Moran MA. Overview of the marine Roseobacter lineage. Appl Environ Microbiol 2005; 71:5665–5677 [View Article] [PubMed]
    [Google Scholar]
  4. Luo H, Moran MA. Evolutionary ecology of the marine Roseobacter clade. Microbiol Mol Biol Rev 2014; 78:573–587 [View Article] [PubMed]
    [Google Scholar]
  5. Wietz M, Gram L, Jørgensen B, Schramm A. Latitudinal patterns in the abundance of major marine bacterioplankton groups. Aquat Microb Ecol 2010; 61:179–189 [View Article]
    [Google Scholar]
  6. Giebel H-A, Kalhoefer D, Lemke A, Thole S, Gahl-Janssen R et al. Distribution of Roseobacter RCA and SAR11 lineages in the North Sea and characteristics of an abundant RCA isolate. ISME J 2011; 5:8–19 [View Article] [PubMed]
    [Google Scholar]
  7. Hahnke S, Brock NL, Zell C, Simon M, Dickschat JS et al. Physiological diversity of Roseobacter clade bacteria co-occurring during a phytoplankton bloom in the North Sea. Syst Appl Microbiol 2013; 36:39–48 [View Article] [PubMed]
    [Google Scholar]
  8. Teeling H, Fuchs BM, Bennke CM, Krüger K, Chafee M et al. Recurring patterns in bacterioplankton dynamics during coastal spring algae blooms. eLife 2016; 5:e11888 [View Article] [PubMed]
    [Google Scholar]
  9. Bakenhus I, Dlugosch L, Billerbeck S, Giebel H-A, Milke F et al. Composition of total and cell-proliferating bacterioplankton community in early summer in the North Sea - Roseobacters are the most active component. Front Microbiol 2017; 8:1771 [View Article] [PubMed]
    [Google Scholar]
  10. Wagner-Döbler I, Biebl H. Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol 2006; 60:255–280 [View Article] [PubMed]
    [Google Scholar]
  11. Newton RJ, Griffin LE, Bowles KM, Meile C, Gifford S et al. Genome characteristics of a generalist marine bacterial lineage. ISME J 2010; 4:784–798 [View Article] [PubMed]
    [Google Scholar]
  12. Rosselló-Mora R, Amann R. The species concept for prokaryotes. FEMS Microbiol Rev 2001; 25:39–67 [View Article] [PubMed]
    [Google Scholar]
  13. Sneath PHA. The maintenance of large numbers of strains of microorganisms, and the implications for culture collections. FEMS Microbiol Lett 1977; 1:333–334 [View Article]
    [Google Scholar]
  14. Hahnke S, Tindall BJ, Schumann P, Sperling M, Brinkhoff T et al. Planktotalea frisia gen. nov., sp. nov., isolated from the southern North Sea. Int J Syst Evol Microbiol 2012; 62:1619–1624 [View Article] [PubMed]
    [Google Scholar]
  15. Baym M, Kryazhimskiy S, Lieberman TD, Chung H, Desai MM et al. Inexpensive multiplexed library preparation for megabase-sized genomes. PLoS One 2015; 10:e0128036 [View Article] [PubMed]
    [Google Scholar]
  16. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
    [Google Scholar]
  17. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD et al. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genom Res 2012; 22:568–576 [View Article] [PubMed]
    [Google Scholar]
  18. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  19. Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2013; 14:178–192 [View Article] [PubMed]
    [Google Scholar]
  20. Pagès H, Aboyoun P, Gentleman R, DebRoy S. Biostrings: efficient manipulation of biological strings. R package version 2.66.0 2022 [View Article]
    [Google Scholar]
  21. Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 2016; 428:726–731 [View Article] [PubMed]
    [Google Scholar]
  22. Ludwig W, Strunk O, Westram R, Richter L, Meier H et al. ARB: a software environment for sequence data. Nucleic Acids Res 2004; 32:1363–1371 [View Article] [PubMed]
    [Google Scholar]
  23. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
    [Google Scholar]
  24. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN:a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article] [PubMed]
    [Google Scholar]
  25. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  26. Cashion P, Holder-Franklin MA, McCully J, Franklin M. A rapid method for the base ratio determination of bacterial DNA. Anal Biochem 1977; 81:461–466 [View Article] [PubMed]
    [Google Scholar]
  27. Ley JD, Cattoir H, Reynaerts A. The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 1970; 12:133–142 [View Article]
    [Google Scholar]
  28. Huss VAR, Festl H, Schleifer KH. Studies on the spectrophotometric determination of DNA hybridization from renaturation rates. Syst Appl Microbiol 1983; 4:184–192 [View Article] [PubMed]
    [Google Scholar]
  29. Wagner-Döbler I, Rheims H, Felske A, El-Ghezal A, Flade-Schröder D et al. Oceanibulbus indolifex gen. nov., sp. nov., a North Sea alphaproteobacterium that produces bioactive metabolites. Int J Syst Evol Microbiol 2004; 54:1177–1184 [View Article] [PubMed]
    [Google Scholar]
  30. Brinkhoff T, Bach G, Heidorn T, Liang L, Schlingloff A et al. Antibiotic production by a Roseobacter clade-affiliated species from the German Wadden Sea and its antagonistic effects on indigenous isolates. Appl Environ Microbiol 2004; 70:2560–2565 [View Article] [PubMed]
    [Google Scholar]
  31. Clayton RK. Spectroscopic analysis of bacteriochlorophylls in vitro and in vivo. Photochem Photobiol 1966; 5:669–677 [View Article]
    [Google Scholar]
  32. Murray RGE, Doetsch RN, Robinow CF. Determinative and cytological light microscopy. In Gerhardt P, Murray RGE, Wood WA, Krieg NR. eds Methods for General and Molecular Bacteriology American Society for Microbiology; 1994 pp 21–41
    [Google Scholar]
  33. Smibert RM, Krieg NR. Phenotypic characterization. In Gerhardt P, Murray RGE, Wood WA, Krieg NR. eds Methods for General and Molecular Bacteriology American Society for Microbiology; 1994 pp 607–654
    [Google Scholar]
  34. Tindall BJ. A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 1990; 13:128–130 [View Article]
    [Google Scholar]
  35. Tindall BJ. Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 1990; 66:199–202 [View Article]
    [Google Scholar]
  36. Tindall BJ. Respiratory lipoquinones as biomarkers. In Akkermans AD, van Elsas JD, de Bruijn FJ. eds Molecular Microbial Ecology Manual Kluwer: 1996
    [Google Scholar]
  37. Labrenz M, Collins MD, Lawson PA, Tindall BJ, Braker G et al. Antarctobacter heliothermus gen. nov., sp. nov., a budding bacterium from hypersaline and heliothermal Ekho Lake. Int J Syst Bacteriol 1998; 48:1363–1372 [View Article] [PubMed]
    [Google Scholar]
  38. Strömpl C, Tindall BJ, Jarvis GN, Lünsdorf H, Moore ER et al. 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 1999; 49:1861–1872 [View Article] [PubMed]
    [Google Scholar]
  39. Kim M, Oh H-S, Park S-C, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article] [PubMed]
    [Google Scholar]
  40. Sapp M, Wichels A, Wiltshire KH, Gerdts G. Bacterial community dynamics during the winter-spring transition in the North Sea. FEMS Microbiol Ecol 2007; 59:622–637 [View Article] [PubMed]
    [Google Scholar]
  41. Alfred-Wegener-Institut Helmholtz-Zentrum für Polar- und Meeresforschung Research vessel HEINCKE operated by the Alfred-Wegener-Institute. J Large Scale Res Fac 2017; 3:A120 [View Article]
    [Google Scholar]
  42. Selje N, Simon M. Composition and dynamics of particle-associated and free-living bacterial communities in the Weser estuary, Germany. Aquat Microb Ecol 2003; 30:221–237 [View Article]
    [Google Scholar]
  43. Rink B, Seeberger S, Martens T, Duerselen C D, Simon M et al. Effects of phytoplankton bloom in a coastal ecosystem on the composition of bacterial communities. Aquat Microb Ecol 2007; 48:47–60 [View Article]
    [Google Scholar]
  44. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007; 35:7188–7196 [View Article] [PubMed]
    [Google Scholar]
  45. Giebel H-A, Kalhoefer D, Gahl-Janssen R, Choo Y-J, Lee K et al. 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 System Evol Microbiol 2013; 63:4207–4217 [View Article]
    [Google Scholar]
  46. Selje N, Brinkhoff T, Simon M. Detection of abundant bacteria in the Weser estuary using culture-dependent and culture-independent approaches. Aquat Microb Ecol 2005; 39:17–34 [View Article]
    [Google Scholar]
  47. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O et al. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 1987; 37:463–464 [View Article]
    [Google Scholar]
  48. Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T et al. Re-evaluating prokaryotic species. Nat Rev Microbiol 2005; 3:733–739 [View Article] [PubMed]
    [Google Scholar]
  49. Thornton DCO. Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean. Eur J Phycol 2014; 49:20–46 [View Article]
    [Google Scholar]
  50. Hahnke S, Sperling M, Langer T, Wichels A, Gerdts G et al. Distinct seasonal growth patterns of the bacterium Planktotalea frisia in the North Sea and specific interaction with phytoplankton algae. FEMS Microbiol Ecol 2013; 86:185–199 [View Article] [PubMed]
    [Google Scholar]
  51. Biersmith A, Benner R. Carbohydrates in phytoplankton and freshly produced dissolved organic matter. Mar Chem 1998; 63:131–144 [View Article]
    [Google Scholar]
  52. Bischoff V, Bunk B, Meier-Kolthoff JP, Spröer C, Poehlein A et al. Cobaviruses-a new globally distributed phage group infecting Rhodobacteraceae in marine ecosystems. ISME J 2019; 13:1404–1421 [View Article] [PubMed]
    [Google Scholar]
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