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Volume 73, Issue 6

sp. nov., a fish pathogen, isolated from the Kiel Fjord Open Access

Abstract

A new strain, K08M4, was isolated from the broad-nosed pipefish in the Kiel Fjord. Infection experiments revealed that K08M4 was highly virulent for juvenile pipefish. Cells of strain K08M4 were Gram-stain-negative, curved rod-shaped and motile by means of a single polar flagellum. The strain grew aerobically at 9–40° C, at pH 4–10.5 and it tolerated up to 12 % (w/v) NaCl. The most prevalent (>10 %) cellular fatty acids of K08M4 were C 7 and C. Whole-genome comparisons revealed that K08M4 represents a separate evolutionary lineage that is distinct from other species and falls within the clade. The genome is 4,886,292 bp in size, consists of two circular chromosomes (3,298,328 and 1, 587,964 bp) and comprises 4,178 protein-coding genes and 175 RNA genes. In this study, we describe the phenotypic features of the new isolate and present the annotation and analysis of its complete genome sequence. Based on these data, the new isolate represents a new species for which we propose the name sp. nov. The type strain is K08M4 (=DSM 109818=CECT 30086).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): complete genome sequence , fish pathogen , genomic comparison , Splendidus clade , Vibrio and virulence factors
Funding
This study was supported by the:
  • DFG (Award WE5822/1-2)
    • Principle Award Recipient: CarolinCharlotte Wendling
  • DFG (Award WE5822/1-1)
    • Principle Award Recipient: CarolinCharlotte Wendling
  • DFG (OR4628/4-2)
    • Principle Award Recipient: RothOlivia
© 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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2023-06-29
2024-10-12
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References

  1. Sawabe T, Kita-Tsukamoto K, Thompson FL. Inferring the evolutionary history of vibrios by means of multilocus sequence analysis. J Bacteriol 2007; 189:7932–7936 [View Article] [PubMed]
     [Google Scholar]
  2. Sawabe T, Ogura Y, Matsumura Y, Feng G, Amin AR et al. Updating the Vibrio clades defined by multilocus sequence phylogeny: proposal of eight new clades, and the description of Vibrio tritonius sp. nov. Front Microbiol 2013; 4:414 [View Article] [PubMed]
     [Google Scholar]
  3. Pérez-Cataluña A, Lucena T, Tarazona E, Arahal DR, Macián MC et al. An MLSA approach for the taxonomic update of the Splendidus clade, a lineage containing several fish and shellfish pathogenic Vibrio spp. Syst Appl Microbiol 2016; 39:361–369 [View Article] [PubMed]
     [Google Scholar]
  4. Egidius E. Vibriosis: pathogenicity and pathology. A review. Aquaculture 1987; 67:15–28 [View Article]
     [Google Scholar]
  5. Ina-Salwany MY, Al-Saari N, Mohamad A, Mursidi F-A, Mohd-Aris A et al. Vibriosis in fish: a review on disease development and prevention. J Aquat Anim Health 2019; 31:3–22 [View Article] [PubMed]
     [Google Scholar]
  6. Sugumar G, Nakai T, Hirata Y, Matsubara D, Muroga K. Vibrio splendidus biovar II as the causative agent of bacillary necrosis of Japanese oyster Crassostrea gigas larvae. Dis Aquat Organ 1998; 33:111–118 [View Article] [PubMed]
     [Google Scholar]
  7. Lacoste A, Jalabert F, Malham S, Cueff A, Gélébart F et al. A Vibrio splendidus strain is associated with summer mortality of juvenile oysters Crassostrea gigas in the Bay of Morlaix (North Brittany, France). Dis Aquat Organ 2001; 46:139–145 [View Article] [PubMed]
     [Google Scholar]
  8. Gómez-León J, Villamil L, Lemos ML, Novoa B, Figueras A. Isolation of Vibrio alginolyticus and Vibrio splendidus from aquacultured carpet shell clam (Ruditapes decussatus) larvae associated with mass mortalities. Appl Environ Microbiol 2005; 71:98–104 [View Article] [PubMed]
     [Google Scholar]
  9. Balcázar JL, Gallo-Bueno A, Planas M, Pintado J. Isolation of Vibrio alginolyticus and Vibrio splendidus from captive-bred seahorses with disease symptoms. Antonie van Leeuwenhoek 2010; 97:207–210 [View Article] [PubMed]
     [Google Scholar]
  10. Baffone W, Pianetti A, Bruscolini F, Barbieri E, Citterio B. Occurrence and expression of virulence-related properties of Vibrio species isolated from widely consumed seafood products. Int J Food Microbiol 2000; 54:9–18 [View Article] [PubMed]
     [Google Scholar]
  11. Su YC, Liu C. Vibrio parahaemolyticus: a concern of seafood safety. Food Microbiol 2007; 24:549–558 [View Article] [PubMed]
     [Google Scholar]
  12. Weinbauer MG, Brettar I, Höfle MG. Lysogeny and virus‐induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol Oceanogr 2003; 48:1457–1465 [View Article]
     [Google Scholar]
  13. O’Shea YA, Boyd EF. Mobilization of the Vibrio pathogenicity island between Vibrio cholerae isolates mediated by CP-T1 generalized transduction. FEMS Microbiol Lett 2002; 214:153–157 [View Article] [PubMed]
     [Google Scholar]
  14. Wendling CC, Batista FM, Wegner KM. Persistence, seasonal dynamics and pathogenic potential of Vibrio communities from Pacific oyster hemolymph. PLoS One 2014; 9:e94256 [View Article] [PubMed]
     [Google Scholar]
  15. Poirier M, Listmann L, Roth O. Selection by higher-order effects of salinity and bacteria on early life-stages of Western Baltic spring-spawning herring. Evol Appl 2017; 10:603–615 [View Article] [PubMed]
     [Google Scholar]
  16. Nasfi H, Travers MA, de Lorgeril J, Habib C, Sannie T et al. A European epidemiological survey of Vibrio splendidus clade shows unexplored diversity and massive exchange of virulence factors. World J Microbiol Biotechnol 2015; 31:461–475 [View Article]
     [Google Scholar]
  17. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
     [Google Scholar]
  18. Roth O, Keller I, Landis SH, Salzburger W, Reusch TBH. Hosts are ahead in a marine host-parasite coevolutionary arms race: innate immune system adaptation in pipefish Syngnathus typhle against Vibrio phylotypes. Evolution 2012; 66:2528–2539 [View Article] [PubMed]
     [Google Scholar]
  19. Wendling CC, Piecyk A, Refardt D, Chibani C, Hertel R et al. Tripartite species interaction: eukaryotic hosts suffer more from phage susceptible than from phage resistant bacteria. BMC Evol Biol 2017; 17:98 [View Article] [PubMed]
     [Google Scholar]
  20. Chibani CM, Hertel R, Hoppert M, Liesegang H, Wendling CC. Closely related Vibrio alginolyticus strains encode an identical repertoire of caudovirales-like regions and filamentous phages. Viruses 2020; 12:1359 [View Article] [PubMed]
     [Google Scholar]
  21. Cerny G. Method for the distinction of gramnegative from grampositive bacteria. European J Appl Microbiol 1976; 3:223–225 [View Article]
     [Google Scholar]
  22. Kovacs N. Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 1956; 178:703 [View Article] [PubMed]
     [Google Scholar]
  23. Sasser M. Technical Note 101: Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids Newark, DE: MIDI; 1990
     [Google Scholar]
  24. 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: [View Article] [PubMed]
     [Google Scholar]
  25. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
     [Google Scholar]
  26. Bowers RM, Kyrpides NC, Stepanauskas R, Harmon-Smith M, Doud D et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol 2017; 35:725–731 [View Article] [PubMed]
     [Google Scholar]
  27. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
     [Google Scholar]
  28. Blum M, Chang H-Y, Chuguransky S, Grego T, Kandasaamy S et al. The InterPro protein families and domains database: 20 years on. Nucleic Acids Res 2021; 49:D344–D354 [View Article] [PubMed]
     [Google Scholar]
  29. Galperin MY, Wolf YI, Makarova KS, Vera Alvarez R, Landsman D et al. COG database update: focus on microbial diversity, model organisms, and widespread pathogens. Nucleic Acids Res 2021; 49:D274–D281 [View Article] [PubMed]
     [Google Scholar]
  30. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–21 [View Article] [PubMed]
     [Google Scholar]
  31. 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]
  32. 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]
  33. 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]
  34. Lefort V, Desper R, Gascuel O. FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 2015; 32:2798–2800 [View Article] [PubMed]
     [Google Scholar]
  35. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–668 [View Article]
     [Google Scholar]
  36. Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V et al. Complete genome sequence of DSM 30083(T), the type strain (U5/41(T)) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genomic Sci 2014; 9:2 [View Article] [PubMed]
     [Google Scholar]
  37. 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]
  38. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 2016; 8:12–24 [View Article]
     [Google Scholar]
  39. Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk v2: memory friendly classification with the genome taxonomy database. Bioinformatics 2022; 38:5315–5316 [View Article] [PubMed]
     [Google Scholar]
  40. Parks DH, Chuvochina M, Rinke C, Mussig AJ, Chaumeil P-A et al. GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Res 2022; 50:D785–D794 [View Article] [PubMed]
     [Google Scholar]
  41. Beemelmanns A, Roth O. Biparental immune priming in the pipefish Syngnathus typhle. Zoology 2016; 119:262–272 [View Article] [PubMed]
     [Google Scholar]
  42. Chibani CM, Roth O, Liesegang H, Wendling CC. Genomic variation among closely related Vibrio alginolyticus strains is located on mobile genetic elements. BMC Genomics 2020; 21:354 [View Article] [PubMed]
     [Google Scholar]
  43. Thompson FL, Thompson CC, Li Y, Gomez-Gil B, Vandenberghe J et al. Vibrio kanaloae sp. nov., Vibrio pomeroyi sp. nov. and Vibrio chagasii sp. nov., from sea water and marine animals. Int J Syst Evol Microbiol 2003; 53:753–759 [View Article] [PubMed]
     [Google Scholar]
  44. Beaz-Hidalgo R, Doce A, Pascual J, Toranzo AE, Romalde JL. Vibrio gallaecicus sp. nov. isolated from cultured clams in north-western Spain. Syst Appl Microbiol 2009; 32:111–117 [View Article]
     [Google Scholar]
  45. Wang H, Liu J, Wang Y, Zhang XH. Vibrio marisflavi sp. nov., isolated from seawater. Int J Syst Evol Microbiol 2011; 61:568–573 [View Article]
     [Google Scholar]
  46. Colwell RR. Polyphasic taxonomy of the genus Vibrio: numerical taxonomy of Vibrio cholerae, Vibrio parahaemolyticus, and related Vibrio species. J Bacteriol 1970; 104:410–433 [View Article] [PubMed]
     [Google Scholar]
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Vibrio syngnathi sp. nov., a fish pathogen, isolated from the Kiel Fjord
Int J Syst Evol Microbiol 73, 005951 (2023); https://doi.org/10.1099/ijsem.0.005951
/content/journal/ijsem/10.1099/ijsem.0.005951
/content/journal/ijsem/10.1099/ijsem.0.005951
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