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Abstract

Strain PVT-9a, a novel Gram-stain-negative, aerobic, non-spore-forming, motile-by-gliding and rod-shaped bacterium, was isolated from a skin lesion of Atlantic salmon ( L.) during a tenacibaculosis outbreak that occurred in 2016 at a Chilean fish farm. Phylogenetic analysis based on 16S rRNA gene sequencing confirmed that strain PVT-9a belonged to the genus , being related to the closest type strains KCTC 52419 (98.49 % sequence similarity), JDTF-79 (97.36 %), JDTF-31 (97.29 %) and IFO 15947 (97.15 %). The genome size of strain PVT-9a was 2.73 Mb with a DNA G+C content 31.09 mol%. Average nucleotide identity analysis among 30 species rendered the most similar strains as follows: KCTC 52419 (87.91 %), IFO 15947 (82.47 %), 35/09 (81.08 %), gv TNO006 (80.91 %) and gv TNO010 (80.96 %). Menaquinone MK-6 was the predominant respiratory quinone. The predominant cell fatty acids (>10 %) were iso-C, iso-C G and iso-C 3-OH. Phenotypic, chemotaxonomic and genomic data supported the assignment of strain PVT-9a (=DSM 115155=RGM 3472) as representing a novel species of , for which the name sp. nov. is proposed.

Funding
This study was supported by the:
  • Agencia Nacional de Investigación y Desarrollo (Award FONDECYT 1230068 and FONDAP 1522A0004)
    • Principle Award Recipient: RubenAvendaño-Herrera
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2023-10-31
2024-05-08
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References

  1. Suzuki M. Genus Tenacibaculum. In Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J et al. eds Bergey's Manual of Systematics of Archaea and Bacteria Chichester: John Wiley & Sons, Inc; 2015 pp 1–7
    [Google Scholar]
  2. Avendaño-Herrera R, Toranzo AE, Magariños B. Tenacibaculosis infection in marine fish caused by Tenacibaculum maritimum: a review. Dis Aquat Org 2006; 71:255–266 [View Article]
    [Google Scholar]
  3. Olsen AB, Powell J, Siah A, Colquhoun DJ, Avendaño-Herrera R. Tenacibaculosis. In Brun E, Rodríguez JF, Macdonald A. eds Technical Report: An Overview of Emerging Diseases in Salmonid Farming Industry Guelph: Aqua Global technical Services Elanco Canada Ltd., Research Park Center; 2019 pp 43–51
    [Google Scholar]
  4. Mabrok M, Algammal AM, Sivaramasamy E, Hetta HF, Atwah B et al. Tenacibaculosis caused by Tenacibaculum maritimum: updated knowledge of this marine bacterial fish pathogen. Front Cell Infect Microbiol 2023; 12:1068000 [View Article]
    [Google Scholar]
  5. Miyake S, Soh M, Azman MN, Ngoh SY, Orbán L et al. Insights into the microbiome of farmed Asian sea bass (Lates calcarifer) with symptoms of tenacibaculosis and description of Tenacibaculum singaporense sp. nov. Antonie van Leeuwenhoek 2020; 113:737–752 [View Article] [PubMed]
    [Google Scholar]
  6. SERNAPESCA Informe sanitario con información sanitaria de agua dulce y marino 2021 (Enero-Noviembre) de salmonicultura en centros marinos; 2021 http://www.sernapesca.cl/sites/default/files/informe_sanitario_con_informacion
  7. Apablaza P, Frisch K, Brevik ØJ, Småge SB, Vallestad C et al. Primary isolation and characterization of Tenacibaculum maritimum from Chilean Atlantic salmon mortalities associated with a Pseudochattonella spp. algal bloom. J Aquat Anim Health 2017; 29:143–149 [View Article] [PubMed]
    [Google Scholar]
  8. Valdes S, Irgang R, Barros MC, Ilardi P, Saldarriaga-Córdoba M et al. First report and characterization of Tenacibaculum maritimum isolates recovered from rainbow trout (Oncorhynchus mykiss) farmed in Chile. J Fish Dis 2021; 44:1481–1490 [View Article] [PubMed]
    [Google Scholar]
  9. Avendaño-Herrera R, Irgang R, Sandoval C, Moreno-Lira P, Houel A et al. Isolation, characterization and virulence potential of Tenacibaculum dicentrarchi in salmonid cultures in Chile. Transbound Emerg Dis 2016; 63:121–126 [View Article] [PubMed]
    [Google Scholar]
  10. Bridel S, Olsen A-B, Nilsen H, Bernardet J-F, Achaz G et al. Comparative genomics of Tenacibaculum dicentrarchi and “Tenacibaculum finnmarkense” highlights intricate evolution of fish-pathogenic species. Genome Biol Evol 2018; 10:452–457 [View Article] [PubMed]
    [Google Scholar]
  11. Avendaño-Herrera R, Saldarriaga-Córdoba M, Irgang R, Newton ILG. Draft genome sequence of Tenacibaculum ovolyticum to-7Br, recovered from a farmed Atlantic salmon (Salmo salar). Microbiol Resour Announc 2022; 11:e0025422 [View Article] [PubMed]
    [Google Scholar]
  12. Avendaño-Herrera R, Olsen AB, Saldarriaga-Cordoba M, Colquhoun DJ, Reyes V et al. Isolation, identification, virulence potential and genomic features of Tenacibaculum piscium isolates recovered from Chilean salmonids. Transbound Emerg Dis 2022; 69:e3305–e3315 [View Article] [PubMed]
    [Google Scholar]
  13. Avendaño‐Herrera R, Collarte C, Saldarriaga‐Córdoba M, Irgang R. New salmonid hosts for Tenacibaculum species: expansion of tenacibaculosis in Chilean aquaculture. J Fish Dis 2020; 43:1077–1085 [View Article]
    [Google Scholar]
  14. Avendaño-Herrera R, Irgang R, Tapia-Cammas D. PCR procedure for detecting the fish pathogen Tenacibaculum dicentrarchi. J Fish Dis 2018; 41:715–719 [View Article] [PubMed]
    [Google Scholar]
  15. Lane DJ. 16S/23S rRNA sequencing. In Stackbrandt E, Goodfellow M. eds Nucleic Acid Techniques in Bacterial Systematics Chichester: Wiley; 1991 pp 115–175
    [Google Scholar]
  16. Hall TA. Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucl Acids Symp Ser 1999; 41:95–98
    [Google Scholar]
  17. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article] [PubMed]
    [Google Scholar]
  18. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  19. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 2018; 35:518–522 [View Article] [PubMed]
    [Google Scholar]
  20. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  21. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003; 19:1572–1574 [View Article] [PubMed]
    [Google Scholar]
  22. Neath AA, Cavanaugh JE. The Bayesian information criterion: background, derivation, and applications. WIREs Computational Stats 2012; 4:199–203 [View Article]
    [Google Scholar]
  23. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  24. Aguilar-Bultet L, Falquet L. Secuenciación y ensmblaje de novo de genomas bacterianos: una alternativa para el studio de nuevos patógenos. Rev Salud Anim 2015; 37:125–132
    [Google Scholar]
  25. Ha SM, Kim CK, Roh J, Byun JH, Yang SJ et al. Application of the whole genome-based bacterial identification system, trueBac ID, using clinical isolates that were not identified with three matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) systems. Ann Lab Med 2019; 39:530–536 [View Article] [PubMed]
    [Google Scholar]
  26. Lee I, Ouk Kim Y, Park SC, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article] [PubMed]
    [Google Scholar]
  27. 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]
  28. 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]
  29. Bertels F, Silander OK, Pachkov M, Rainey PB, van Nimwegen E. Automated reconstruction of whole-genome phylogenies from short-sequence reads. Mol Biol Evol 2014; 31:1077–1088 [View Article] [PubMed]
    [Google Scholar]
  30. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
    [Google Scholar]
  31. Garber AI, Nealson KH, Okamoto A, McAllister SM, Chan CS et al. FeGenie: a comprehensive tool for the identification of iron genes and iron gene neighborhoods in genome and metagenome assemblies. Front Microbiol 2020; 11:37 [View Article] [PubMed]
    [Google Scholar]
  32. Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48:D517–D525 [View Article] [PubMed]
    [Google Scholar]
  33. Liu B, Zheng D, Jin Q, Chen L, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res 2019; 47:D687–D692 [View Article] [PubMed]
    [Google Scholar]
  34. Kim YO, Park IS, Park S, Nam BH, Park JM et al. Tenacibaculum haliotis sp. nov., isolated from the gut of an abalone Haliotis discus hannai. Int J Syst Evol Microbiol 2017; 67:3268–3273 [View Article] [PubMed]
    [Google Scholar]
  35. Olsen AB, Spilsberg B, Nilsen HK, Lagesen K, Gulla S et al. Tenacibaculum piscium sp. nov., isolated from skin ulcers of sea-farmed fish, and description of Tenacibaculum finnmarkense sp. nov. with subdivision into genomovars finnmarkense and ulcerans. Int J Syst Evol Microbiol 2020; 70:6079–6090 [View Article]
    [Google Scholar]
  36. Piñeiro-Vidal M, Gijón D, Zarza C, Santos Y. Tenacibaculum dicentrarchi sp. nov., a marine bacterium of the family Flavobacteriaceae isolated from European sea bass. Int J Syst Evol Microbiol 2012; 62:425–429 [View Article] [PubMed]
    [Google Scholar]
  37. Suzuki M, Nakagawa Y, Harayama S, Yamamoto S. Phylogenetic analysis and taxonomic study of marine Cytophaga-like bacteria: proposal for Tenacibaculum gen. nov. with Tenacibaculum maritimum comb. nov. and Tenacibaculum ovolyticum comb. nov., and description of Tenacibaculum mesophilum sp. nov. and Tenacibaculum amylolyticum sp. nov. Int J Syst Evol Microbiol 2001; 51:1639–1652
    [Google Scholar]
  38. Pazos F, Santos Y, Macias AR, Nunez S, Toranzo AE. Evaluation of media for the successful culture of Flexibacter maritimus. J Fish Diseases 1996; 19:193–197 [View Article]
    [Google Scholar]
  39. Bernardet J-F, Nakagawa Y, Holmes B. Proposed minimal standards for describing new taxa of the family Flavobacteriaceae and emended description of the family. Int J Syst Evol Microbiol 2002; 52:1049–1070 [View Article] [PubMed]
    [Google Scholar]
  40. Lányi B. Classical and rapid identification methods for medically important bacteria. In Colwell R. eds Methods in Microbiology vol 19 Academic Press; 1988 pp 1–67
    [Google Scholar]
  41. Avendaño-Herrera R, Magariños B, López-Romalde S, Romalde JL, Toranzo AE. Phenotypic characterization and description of two major O-serotypes in Tenacibaculum maritimum strains from marine fishes. Dis Aquat Organ 2004; 58:1–8 [View Article] [PubMed]
    [Google Scholar]
  42. 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]
  43. Tindall BJ, Sikorski J, Smibert RM, Kreig NR. Phenotypic characterization and the principles of comparative systematics. In Reddy CA, Beveridge TJ, Breznak JA, Marzluf GA, Schmidt TM et al. eds Methods for General and Molecular Microbiology Wiley; 2007 pp 330–393 [View Article]
    [Google Scholar]
  44. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. In MIDI Technical Note vol 101 MIDI Inc; 1990
    [Google Scholar]
  45. MIDI Sherlock Microbial Identification System Operating Manual. Version 6.1 Newark, DE: MIDI Inc; 2008
    [Google Scholar]
  46. Hansen GH, Bergh O, Michaelsen J, Knappskog D. Flexibacter ovolyticus sp. nov., a pathogen of eggs and larvae of Atlantic halibut, Hippoglossus hippoglossus L. Int J Syst Bacteriol 1992; 42:451–458 [View Article] [PubMed]
    [Google Scholar]
  47. Park S, Choi SJ, Won SM, Yoon JH. Tenacibaculum aestuariivivum sp. nov., isolated from a tidal flat. Int J Syst Evol Microbiol 2017; 67:4612–4618 [View Article] [PubMed]
    [Google Scholar]
  48. Park S, Choi J, Choi SJ, Yoon JH. Tenacibaculum insulae sp. nov., isolated from a tidal flat. Int J Syst Evol Microbiol 2018; 68:228–233 [View Article]
    [Google Scholar]
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