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Volume 73, Issue 10

gen. nov. sp. nov., a diatom symbiont isolated from the phycosphere of Open Access

Abstract

A diatom-associated bacterium, designated as strain F10, was isolated from a pure culture of the pennate diatom A3 and has since been used to characterize molecular mechanisms of symbiosis between phytoplankton and bacteria, including interactions using diatom-derived azelaic acid. Its origin from a hypersaline environment, combined with its capacity for quorum sensing, biofilm formation, and potential for dimethylsulfoniopropionate methylation/cleavage, suggest it is within the family . Initial phylogenetic analysis of the 16S rRNA gene sequence placed this isolate within the genus, but recent genomic and phylogenomic analyses show strain F10 is a separate lineage diverging from the genus . The genomic DNA G+C content is 60.0 mol%. The predominant respiratory quinone is Q-10. The major fatty acids are C ω7 and C. Strain F10 also contains C3-OH and the furan-containing fatty acid 10,13-epoxy-11-methyl-octadecadienoate (9-(3-methyl-5-pentylfuran-2-yl)nonanoic acid). The major polar lipids are diphosphatidylglycerol, phosphatidylethanolamine and phosphatidylglycerol. Based on genomic, phylogenomic, phenotypic and chemotaxonomic characterizations, strain F10 represents a novel genus and species with the proposed name, gen. nov. sp. nov. The type strain is F10 (=NCMA B37=NCIMB 15470=NRIC 2002).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): diatom–bacteria symbiosis , phycosphere and Roseobacter
Funding
This study was supported by the:
  • Research Institute Centers, New York University Abu Dhabi (Award ADHPG-CG009)
    • Principle Award Recipient: ShadyA. Amin
  • Gordon and Betty Moore Foundation (Award GBMF9335)
    • Principle Award Recipient: ShadyA. Amin
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2023-10-27
2024-05-02
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References

  1. 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: [View Article]
     [Google Scholar]
  2. Oren A, Garrity GM. Valid publication of new names and new combinations effectively published outside the IJSEM. Int J Syst Evol Microbiol 2021; 71: [View Article]
     [Google Scholar]
  3. Geng H, Belas R. Molecular mechanisms underlying Roseobacter-phytoplankton symbioses. Curr Opin Biotechnol 2010; 21:332–338 [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. Behringer G, Ochsenkühn MA, Fei C, Fanning J, Koester JA et al. Bacterial communities of diatoms display strong conservation across strains and time. Front Microbiol 2018; 9:659 [View Article] [PubMed]
     [Google Scholar]
  6. Fei C, Ochsenkühn MA, Shibl AA, Isaac A, Wang C et al. Quorum sensing regulates “swim-or-stick” lifestyle in the phycosphere. Environ Microbiol 2020; 22:4761–4778 [View Article] [PubMed]
     [Google Scholar]
  7. Shibl AA, Isaac A, Ochsenkühn MA, Cárdenas A, Fei C et al. Diatom modulation of select bacteria through use of two unique secondary metabolites. Proc Natl Acad Sci USA 2020; 117:27445–27455 [View Article] [PubMed]
     [Google Scholar]
  8. Shibl AA, Ochsenkühn MA, Mohamed AR, Isaac A, Coe LSY et al. Molecular mechanisms of microbiome modulation by the eukaryotic secondary metabolite azelaic acid. eLife 2023; 12:RP88525 [View Article]
     [Google Scholar]
  9. Kim M, Oh HS, Park SC, 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]
  10. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article] [PubMed]
     [Google Scholar]
  11. Hofmann MA, Brian DA. Sequencing PCR DNA amplified directly from a bacterial colony. Biotechniques 1991; 11:30–31 [PubMed]
     [Google Scholar]
  12. Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 2015; 522:98–101 [View Article] [PubMed]
     [Google Scholar]
  13. 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]
  14. Meier-Kolthoff JP, Sard Carbasse J, 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]
  15. Na SI, Kim YO, Yoon SH, Ha SM, 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]
  16. Edler D, Klein J, Antonelli A, Silvestro D, Matschiner M. raxmlGUI 2.0: a graphical interface and toolkit for phylogenetic analyses using RAxML. Methods Ecol Evol 2021; 12:373–377 [View Article]
     [Google Scholar]
  17. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article] [PubMed]
     [Google Scholar]
  18. Lee MD. GToTree: a user-friendly workflow for phylogenomics. Bioinformatics 2019; 35:4162–4164 [View Article] [PubMed]
     [Google Scholar]
  19. Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
     [Google Scholar]
  20. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 2016 [View Article]
     [Google Scholar]
  21. 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; 14:1–4 [View Article] [PubMed]
     [Google Scholar]
  22. ZoBell CE. Studies on marine bacteria. I. The cultural requirements of heterotrophic aerobes. J Mar Res 1941; 4:42–75
     [Google Scholar]
  23. Sonnenschein EC, Phippen CBW, Nielsen KF, Mateiu RV, Melchiorsen J et al. Phaeobacter piscinae sp. nov., a species of the Roseobacter group and potential aquaculture probiont. Int J Syst Evol Microbiol 2017; 67:4559–4564 [View Article] [PubMed]
     [Google Scholar]
  24. 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]
  25. Buck JD. Nonstaining (KOH) method for determination of Gram reactions of marine bacteria. Appl Environ Microbiol 1982; 44:992–993 [View Article] [PubMed]
     [Google Scholar]
  26. Breider S, Scheuner C, Schumann P, Fiebig A, Petersen J et al. Genome-scale data suggest reclassifications in the Leisingera-Phaeobacter cluster including proposals for Sedimentitalea gen. nov. and Pseudophaeobacter gen. nov. Front Microbiol 2014; 5:416 [View Article] [PubMed]
     [Google Scholar]
  27. Wirth JS, Whitman WB. Phylogenomic analyses of a clade within the roseobacter group suggest taxonomic reassignments of species of the genera Aestuariivita, Citreicella, Loktanella, Nautella, Pelagibaca, Ruegeria, Thalassobius, Thiobacimonas and Tropicibacter, and the proposal of six novel genera. Int J Syst Evol Microbiol 2018; 68:2393–2411 [View Article] [PubMed]
     [Google Scholar]
  28. Hördt A, López MG, Meier-Kolthoff JP, Schleuning M, Weinhold L-M et al. Analysis of 1,000+ type-strain genomes substantially improves taxonomic classification of Alphaproteobacteria. Front Microbiol 2020; 11:468 [View Article] [PubMed]
     [Google Scholar]
  29. Konstantinidis KT, Tiedje JM. Towards a genome-based taxonomy for prokaryotes. J Bacteriol 2005; 187:6258–6264 [View Article] [PubMed]
     [Google Scholar]
  30. Zhang DC, Li HR, Xin YH, Liu HC, Chi ZM et al. Phaeobacter arcticus sp. nov., a psychrophilic bacterium isolated from the Arctic. Int J Syst Evol Microbiol 2008; 58:1384–1387 [View Article] [PubMed]
     [Google Scholar]
  31. Gaboyer F, Tindall BJ, Ciobanu MC, Duthoit F, Le Romancer M et al. Phaeobacter leonis sp. nov., an alphaproteobacterium from Mediterranean sea sediments. Int J Syst Evol Microbiol 2013; 63:3301–3306 [View Article] [PubMed]
     [Google Scholar]
  32. Yoon JH, Kang SJ, Lee SY, Oh TK. Phaeobacter daeponensis sp. nov., isolated from a tidal flat of the Yellow sea in Korea. Int J Syst Evol Microbiol 2007; 57:856–861 [View Article]
     [Google Scholar]
  33. Breider S, Freese HM, Spröer C, Simon M, Overmann J et al. Phaeobacter porticola sp. nov., an antibiotic-producing bacterium isolated from a sea harbour. Int J Syst Evol Microbiol 2017; 67:2153–2159 [View Article] [PubMed]
     [Google Scholar]
  34. Guan Y, Jiang Y, Kim YM, Yu SY, Choi SH et al. Pseudophaeobacter flagellatus sp. nov., isolated from coastal water. Int J Syst Evol Microbiol 2022; 72: [View Article] [PubMed]
     [Google Scholar]
  35. Park S, Park DS, Bae KS, Yoon JH. Phaeobacter aquaemixtae sp. nov., isolated from the junction between the ocean and a freshwater spring. Int J Syst Evol Microbiol 2014; 64:1378–1383 [View Article] [PubMed]
     [Google Scholar]
  36. 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., reclassificationof 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]
     [Google Scholar]
  37. Vandecandelaere I, Nercessian O, Faimali M, Segaert E, Mollica A et al. Bacterial diversity of the cultivable fraction of a marine electroactive biofilm. Bioelectrochemistry 2010; 78:62–66 [View Article] [PubMed]
     [Google Scholar]
  38. Vandecandelaere I, Segaert E, Mollica A, Faimali M, Vandamme P. Phaeobacter caeruleus sp. nov., a blue-coloured, colony-forming bacterium isolated from a marine electroactive biofilm. Int J Syst Evol Microbiol 2009; 59:1209–1214 [View Article] [PubMed]
     [Google Scholar]
  39. Vandecandelaere I, Segaert E, Mollica A, Faimali M, Vandamme P. Leisingera aquimarina sp. nov., isolated from a marine electroactive biofilm, and emended descriptions of Leisingera methylohalidivorans Schaefer et al. 2002, Phaeobacter daeponensis Yoon et al. 2007 and Phaeobacter inhibens Martens et al. 2006. Int J Syst Evol Microbiol 2008; 58:2788–2793 [View Article] [PubMed]
     [Google Scholar]
  40. Lemke RAS, Peterson AC, Ziegelhoffer EC, Westphall MS, Tjellström H et al. Synthesis and scavenging role of furan fatty acids. Proc Natl Acad Sci USA 2014; 111:E3450–E3457 [View Article] [PubMed]
     [Google Scholar]
  41. Schaefer JK, Goodwin KD, McDonald IR, Murrell JC. Leisingera methylohalidivorans gen. nov., sp. nov., a marine methylotroph that grows on methyl bromide. Int J Syst Evol Microbiol 2002; 52:851–859 [View Article]
     [Google Scholar]
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Phycobacter azelaicus gen. nov. sp. nov., a diatom symbiont isolated from the phycosphere of Asterionellopsis glacialis
Int J Syst Evol Microbiol 73, 006104 (2023); https://doi.org/10.1099/ijsem.0.006104
/content/journal/ijsem/10.1099/ijsem.0.006104
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