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Abstract

A Gram-negative, aerobic, pink-pigmented, and bacteriochlorophyll -containing bacterial strain, designated B14, was isolated from the macroalga sampled from the southern North Sea, Germany. Based on 16S rRNA gene sequences, species of the genera and were most closely related to strain B14 with sequence identities ranging from 98.15 % ( Och 114) to 99.11 % ( Och 149), whereas CH-B427 exhibited 98.52 % sequence identity. Digital DNA–DNA hybridization and average nucleotide identity values between the genome of the novel strain and that of closely related and type strains were <20 % and <77 %, respectively. The novel strain contained ubiquinone-10 as the only respiratory quinone and C ω7, C, C, C ω7, C ω7,13, and C 3-OH as the major cellular fatty acids. The predominant polar lipids of strain B14 were phosphatidylcholine, phosphatidylethanolamine, and phosphatidylglycerol. The genome of strain B14 comprises a chromosome with a size of 4.5 Mbp, one chromid, and four plasmids. The genome contains the complete gene cluster for aerobic anoxygenic photosynthesis required for a photoheterotrophic lifestyle. The results of this study indicate that strain B14 (=DSM 116946=LMG 33352) represents a novel species of the genus for which the name sp. nov. is proposed.

Funding
This study was supported by the:
  • Deutsche Forschungsgemeinschaft (Award 451574234)
    • Principle Award Recipient: ThorstenBrinkhoff
  • Deutsche Forschungsgemeinschaft (Award TRR 51)
    • Principle Award Recipient: JörnPetersen
  • Deutsche Forschungsgemeinschaft (Award TRR 51)
    • Principle Award Recipient: RolfDaniel
  • Deutsche Forschungsgemeinschaft (Award TRR 51)
    • Principle Award Recipient: ThorstenBrinkhoff
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2024-06-11
2024-06-19
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References

  1. Shiba T. Roseobacter litoralis gen. nov., sp. nov., and Roseobacter denitrificans sp. nov., aerobic pink-pigmented bacteria which contain bacteriochlorophyll a. Syst Appl Microbiol 1991; 14:140–145 [View Article] [PubMed]
    [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. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
    [Google Scholar]
  4. Jung Y-T, Park S, Lee J-S, Yoon J-H. Roseobacter ponti sp. nov., isolated from seawater. Int J Syst Evol Microbiol 2017; 67:2189–2194 [View Article] [PubMed]
    [Google Scholar]
  5. Muramatsu S, Kanamuro M, Sato-Takabe Y, Hirose S, Muramatsu Y et al. Roseobacter cerasinus sp. nov., isolated from a fish farm. Int J Syst Evol Microbiol 2020; 70:4920–4926 [View Article] [PubMed]
    [Google Scholar]
  6. Lee EB, Park S, Kim W, Yoon J-H. Roseobacter insulae sp. nov. and Loktanella gaetbuli sp. nov., isolated from tidal flats in the Yellow Sea in Korea. Int J Syst Evol Microbiol 2023; 73:5794 [View Article]
    [Google Scholar]
  7. Yurkov VV, Beatty JT. Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 1998; 62:695–724 [View Article]
    [Google Scholar]
  8. Zheng Q, Zhang R, Koblížek M, Boldareva EN, Yurkov V et al. Diverse arrangement of photosynthetic gene clusters in aerobic anoxygenic phototrophic bacteria. PLoS One 2011; 6:e25050 [View Article] [PubMed]
    [Google Scholar]
  9. Brinkmann H, Göker M, Koblížek M, Wagner-Döbler I, Petersen J. Horizontal operon transfer, plasmids, and the evolution of photosynthesis in Rhodobacteraceae. ISME J 2018; 12:1994–2010 [View Article] [PubMed]
    [Google Scholar]
  10. Liu Y, Zheng Q, Lin W, Jiao N. Characteristics and evolutionary analysis of photosynthetic gene clusters on extrachromosomal replicons: from streamlined plasmids to chromids. mSystems 2019; 4:e00358–19 [View Article]
    [Google Scholar]
  11. Dogs M, Wemheuer B, Wolter L, Bergen N, Daniel R et al. Rhodobacteraceae on the marine brown alga Fucus spiralis are abundant and show physiological adaptation to an epiphytic lifestyle. Syst Appl Microbiol 2017; 40:370–382 [View Article] [PubMed]
    [Google Scholar]
  12. Zech H, Thole S, Schreiber K, Kalhöfer D, Voget S et al. Growth phase-dependent global protein and metabolite profiles of Phaeobacter gallaeciensis strain DSM 17395, a member of the marine Roseobacter-clade. Proteomics 2009; 9:3677–3697 [View Article] [PubMed]
    [Google Scholar]
  13. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  14. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  15. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
    [Google Scholar]
  16. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
    [Google Scholar]
  17. García-Alcalde F, Okonechnikov K, Carbonell J, Cruz LM, Götz S et al. Qualimap: evaluating next-generation sequencing alignment data. Bioinformatics 2012; 28:2678–2679 [View Article] [PubMed]
    [Google Scholar]
  18. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 2018; 34:3094–3100 [View Article]
    [Google Scholar]
  19. Na S-I, Kim YO, Yoon S-H, Ha S, Baek I et al. UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 2018; 56:280–285 [View Article]
    [Google Scholar]
  20. Philippe H. MUST, a computer package of management utilities for sequences and trees. Nucleic Acids Res 1993; 21:5264–5272 [View Article] [PubMed]
    [Google Scholar]
  21. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007; 56:564–577 [View Article] [PubMed]
    [Google Scholar]
  22. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
    [Google Scholar]
  23. 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]
  24. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
    [Google Scholar]
  25. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 2006; 33:152–154
    [Google Scholar]
  26. 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]
  27. Auch AF, von Jan M, Klenk H-P, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010; 2:117–134 [View Article] [PubMed]
    [Google Scholar]
  28. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  29. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114 [View Article] [PubMed]
    [Google Scholar]
  30. Petersen J, Vollmers J, Ringel V, Brinkmann H, Ellebrandt-Sperling C et al. A marine plasmid hitchhiking vast phylogenetic and geographic distances. Proc Natl Acad Sci U S A 2019; 116:20568–20573 [View Article] [PubMed]
    [Google Scholar]
  31. Harrison PW, Lower RPJ, Kim NKD, Young JPW. Introducing the bacterial “chromid”: not a chromosome, not a plasmid. Trends Microbiol 2010; 18:141–148 [View Article] [PubMed]
    [Google Scholar]
  32. Petersen J, Frank O, Göker M, Pradella S. Extrachromosomal, extraordinary and essential--the plasmids of the Roseobacter clade. Appl Microbiol Biotechnol 2013; 97:2805–2815 [View Article] [PubMed]
    [Google Scholar]
  33. Birmes L, Freese HM, Petersen J. RepC_soli: a novel promiscuous plasmid type of Rhodobacteraceae mediates horizontal transfer of antibiotic resistances in the ocean. Environ Microbiol 2021; 23:5395–5411 [View Article] [PubMed]
    [Google Scholar]
  34. Kalhoefer D, Thole S, Voget S, Lehmann R, Liesegang H et al. Comparative genome analysis and genome-guided physiological analysis of Roseobacter litoralis. BMC Genomics 2011; 12:324 [View Article] [PubMed]
    [Google Scholar]
  35. Frank O, Michael V, Päuker O, Boedeker C, Jogler C et al. Plasmid curing and the loss of grip--the 65-kb replicon of Phaeobacter inhibens DSM 17395 is required for biofilm formation, motility and the colonization of marine algae. Syst Appl Microbiol 2015; 38:120–127 [View Article] [PubMed]
    [Google Scholar]
  36. Michael V, Frank O, Bartling P, Scheuner C, Göker M et al. Biofilm plasmids with a rhamnose operon are widely distributed determinants of the “swim-or-stick” lifestyle in roseobacters. ISME J 2016; 10:2498–2513 [View Article] [PubMed]
    [Google Scholar]
  37. Urvoy M, Labry C, L’Helguen S, Lami R. Quorum sensing regulates bacterial processes that play a major role in marine biogeochemical cycles. Front Mar Sci 2022; 9:834337 [View Article]
    [Google Scholar]
  38. Berger M, Neumann A, Schulz S, Simon M, Brinkhoff T. Tropodithietic acid production in Phaeobacter gallaeciensis is regulated by N-acyl homoserine lactone-mediated quorum sensing. J Bacteriol 2011; 193:6576–6585 [View Article] [PubMed]
    [Google Scholar]
  39. Ha D-G, Kuchma SL, O’Toole GA. Plate-based assay for swimming motility in Pseudomonas aeruginosa. Methods Mol Biol 2014; 1149:59–65 [View Article] [PubMed]
    [Google Scholar]
  40. Rashid MH, Kornberg A. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 2000; 97:4885–4890 [View Article] [PubMed]
    [Google Scholar]
  41. Kovacs N. Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 1956; 178:703 [View Article] [PubMed]
    [Google Scholar]
  42. Barrow GI, Feltham RKA. Cowan and Steel’s Manual for Identification of Medical Bacteria, 3rd. edn Cambridge: Cambridge University Press; 1993
    [Google Scholar]
  43. Lányi B. Classical and rapid identification methods for medically important bacteria. Methods Microbiol 1987; 19:1–67 [View Article]
    [Google Scholar]
  44. Wolter LA, Wietz M, Ziesche L, Breider S, Leinberger J et al. Pseudooceanicola algae sp. nov., isolated from the marine macroalga Fucus spiralis, shows genomic and physiological adaptations for an algae-associated lifestyle. Syst Appl Microbiol 2021; 44:126166 [View Article] [PubMed]
    [Google Scholar]
  45. CLSI Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard, 12th. edn CLSI Document M02-A11; 2015
    [Google Scholar]
  46. Vieira S, Huber KJ, Neumann-Schaal M, Geppert A, Luckner M et al. Usitatibacter rugosus gen. nov., sp. nov. and Usitatibacter palustris sp. nov., novel members of Usitatibacteraceae fam. nov. within the order Nitrosomonadales isolated from soil. Int J Syst Evol Microbiol 2021; 71:004631 [View Article] [PubMed]
    [Google Scholar]
  47. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37:911–917 [View Article] [PubMed]
    [Google Scholar]
  48. Tindall BJ, Sikorski J, Smibert RM, Krieg NR. Phenotypic characterization and the principles of comparative systematics. In Methods for General and Molecular Microbiology, 3rd. edn Washington, DC: American Society for Microbiology Press; 2007 pp 330–393 [View Article]
    [Google Scholar]
  49. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. In MIDI Technical Note 101 Newark: MIDI, Inc; 1990
    [Google Scholar]
  50. Martens T, Heidorn T, Pukall R, Simon M, Tindall BJ et al. 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 2006; 56:1293–1304 [View Article] [PubMed]
    [Google Scholar]
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