1887

Abstract

A polyphasic study was undertaken to clarify the taxonomic position of strains isolated from Atlantic salmon () cage-farmed in Chile. Four salmon and three seal isolates showed minor differences in the SDS-PAGE protein analysis. Thus, a major protein band present in the salmon isolates, of approximately 22.4 kDa, was absent in the pinniped strains, regardless of the growth media employed. In addition, the pinniped strains showed protein bands with molecular masses of 71.5 and 14.2 kDa, when grown on trypticase soy agar supplemented with 1 % NaCl, or 25.6 kDa, when grown on Columbia blood agar, not present in the Atlantic salmon strains. A high similarity in the matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) MS spectra of the strains was observed, although some minor peaks were absent in the fish isolates. Fatty acid methyl esters from isolates with different host origin significantly (<0.05) differed in the content of C, C, Cω9, Cω6,9,12,15 and summed features 3, 5 and 8. The salmon isolates formed a separate cluster in the phylogenetic analysis of housekeeping genes, separately or as concatenated sequences. Sequence divergences among salmon and seal strains were in the range of inter-subspecies differentiation for (2.5 %), (1.8 %), (2.1 %), (1.7 %) and (2.0 %) genes. DNA–DNA hybridization results confirmed those of sequencing, showing reassociation values between seal and salmon strains close to the borderline of species definition. Differences in growth at low temperatures and in the haemolytic capacities were also observed between both groups of isolates. On the basis of all these results, the salmon isolates represent a novel subspecies of , for which the name subsp. subsp. nov. is proposed. The type strain is C-4 ( = CECT 7921 = DSM 24768). The subspecies subsp. subsp. nov. is automatically created. An emended description of is also provided.

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2014-05-01
2020-01-25
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References

  1. Alber J. , El-Sayed A. , Lämmler C. , Hassan A. A. , Vossen A. , Siebert U. . ( 2004; ). Determination of species-specific sequences of superoxide dismutase A encoding gene sodA and chaperonin 60 encoding gene cpn60 for identification and phylogenetic analysis of Streptococcus phocae . . Vet Microbiol 101:, 117–122. [CrossRef] [PubMed]
    [Google Scholar]
  2. Baele M. , Storms V. , Haesebrouck F. , Devriese L. A. , Gillis M. , Verschraegen G. , de Baere T. , Vaneechoutte M. . ( 2001; ). Application and evaluation of the interlaboratory reproducibility of tRNA intergenic length polymorphism analysis (tDNA-PCR) for identification of Streptococcus species. . J Clin Microbiol 39:, 1436–1442. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bentley R. W. , Leigh J. A. . ( 1995; ). Development of PCR-based hybridization protocol for identification of streptococcal species. . J Clin Microbiol 33:, 1296–1301.[PubMed]
    [Google Scholar]
  4. Bentley R. W. , Leigh J. A. , Collins M. D. . ( 1991; ). Intrageneric structure of Streptococcus based on comparative analysis of small-subunit rRNA sequences. . Int J Syst Bacteriol 41:, 487–494. [CrossRef] [PubMed]
    [Google Scholar]
  5. Chatellier S. , Harel J. , Zhang Y. , Gottschalk M. , Higgins R. , Devriese L. A. , Brousseau R. . ( 1998; ). Phylogenetic diversity of Streptococcus suis strains of various serotypes as revealed by 16S rRNA gene sequence comparison. . Int J Syst Bacteriol 48:, 581–589. [CrossRef] [PubMed]
    [Google Scholar]
  6. Davies A. P. , Reid M. , Hadfield S. J. , Johnston S. , Mikhail J. , Harris L. G. , Jenkinson H. F. , Berry N. , Lewis A. M. . & other authors ( 2012; ). Identification of clinical isolates of α-hemolytic streptococci by 16S rRNA gene sequencing, matrix-assisted laser desorption ionization-time of flight mass spectrometry using MALDI Biotyper, and conventional phenotypic methods: a comparison. . J Clin Microbiol 50:, 4087–4090. [CrossRef] [PubMed]
    [Google Scholar]
  7. Facklam R. . ( 2002; ). What happened to the streptococci: overview of taxonomic and nomenclature changes. . Clin Microbiol Rev 15:, 613–630. [CrossRef] [PubMed]
    [Google Scholar]
  8. Gibello A. , Mata A. I. , Blanco M. M. , Casamayor A. , Domínguez L. , Fernández-Garayzabal J. F. . ( 2005; ). First identification of Streptococcus phocae isolated from Atlantic salmon (Salmo salar). . J Clin Microbiol 43:, 526–527. [CrossRef] [PubMed]
    [Google Scholar]
  9. Gillespie B. E. , Jayarao B. M. , Oliver S. P. . ( 1997; ). Identification of Streptococcus species by randomly amplified polymorphic deoxyribonucleic acid fingerprinting. . J Dairy Sci 80:, 471–476. [CrossRef] [PubMed]
    [Google Scholar]
  10. Glazunova O. O. , Raoult D. , Roux V. . ( 2009; ). Partial sequence comparison of the rpoB, sodA, groEL and gyrB genes within the genus Streptococcus . . Int J Syst Evol Microbiol 59:, 2317–2322. [CrossRef] [PubMed]
    [Google Scholar]
  11. Glazunova O. O. , Raoult D. , Roux V. . ( 2010; ). Partial recN gene sequencing: a new tool for identification and phylogeny within the genus Streptococcus . . Int J Syst Evol Microbiol 60:, 2140–2148. [CrossRef] [PubMed]
    [Google Scholar]
  12. Hassan A. A. , Khan I. U. , Abdulmawjood A. , Lämmler C. . ( 2003; ). Inter- and intraspecies variations of the 16S–23S rDNA intergenic spacer region of various streptococcal species. . Syst Appl Microbiol 26:, 97–103. [CrossRef] [PubMed]
    [Google Scholar]
  13. Henton M. M. , Zapke O. , Basson P. A. . ( 1999; ). Streptococcus phocae infections associated with starvation in Cape fur seals. . J S Afr Vet Assoc 70:, 98–99. [CrossRef] [PubMed]
    [Google Scholar]
  14. Hueffer K. , Lieske C. L. , McGilvary L. M. , Hare R. F. , Miller D. L. , O’Hara T. M. . ( 2011; ). Streptococcus phocae isolated from a spotted seal (Phoca largha) with pyometra in Alaska. . J Zoo Wildl Med 42:, 108–112. [CrossRef] [PubMed]
    [Google Scholar]
  15. Ikryannikova L. N. , Filimonova A. V. , Malakhova M. V. , Savinova T. , Filimonova O. , Ilina E. N. , Dubovickaya V. A. , Sidorenko S. V. , Govorun V. M. . ( 2013; ). Discrimination between Streptococcus pneumoniae and Streptococcus mitis based on sorting of their MALDI mass spectra. . Clin Microbiol Infect 19:, 1066–1071.[PubMed] [CrossRef]
    [Google Scholar]
  16. Imai D. , Jang S. , Miller M. , Conrad P. A. . ( 2009; ). Characterization of beta-hemolytic streptococci isolated from southern sea otters (Enhydra lutris nereis) stranded along the California coast. . Vet Microbiol 136:, 378–381. [CrossRef] [PubMed]
    [Google Scholar]
  17. Johnson S. , Lowenstine L. , Gulland F. , Jang S. , Imai D. , Almy F. , Delong R. , Gardner I. . ( 2006; ). Aerobic bacterial flora of the vagina and prepuce of California sea lions (Zalophus californianus) and investigation of associations with urogenital carcinoma. . Vet Microbiol 114:, 94–103. [CrossRef] [PubMed]
    [Google Scholar]
  18. Kärpänoja P. , Harju I. , Rantakokko-Jalava K. , Haanperä M. , Sarkkinen H. . ( 2013; ). Evaluation of two matrix-assisted laser desorption ionization-time of flight mass spectrometry systems for identification of viridans group streptococci. . Eur J Clin Microbiol Infect Dis. [CrossRef] [PubMed]
    [Google Scholar]
  19. Kawamura Y. , Hou X.-G. , Sultana F. , Miura H. , Ezaki T. . ( 1995; ). Determination of 16S rRNA sequences of Streptococcus mitis and Streptococcus gordonii and phylogenetic relationships among members of the genus Streptococcus . . Int J Syst Bacteriol 45:, 406–408. [CrossRef] [PubMed]
    [Google Scholar]
  20. Kawamura Y. , Whiley R. A. , Shu S. E. , Ezaki T. , Hardie J. M. . ( 1999; ). Genetic approaches to the identification of the mitis group within the genus Streptococcus . . Microbiology 145:, 2605–2613.[PubMed]
    [Google Scholar]
  21. Köhler W. . ( 2007; ). The present state of species within the genera Streptococcus and Enterococcus . . Int J Med Microbiol 297:, 133–150. [CrossRef] [PubMed]
    [Google Scholar]
  22. Kuiken T. , Kennedy S. , Barrett T. , Van de Bildt M. W. G. , Borgsteede F. H. , Brew S. D. , Codd G. A. , Duck C. , Deaville R. . & other authors ( 2006; ). The 2000 canine distemper epidemic in Caspian seals (Phoca caspica): pathology and analysis of contributory factors. . Vet Pathol 43:, 321–338. [CrossRef] [PubMed]
    [Google Scholar]
  23. Laemmli U. K. . ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. . Nature 227:, 680–685. [CrossRef] [PubMed]
    [Google Scholar]
  24. Moon H.-W. , Lee S. H. , Chung H.-S. , Lee M. , Lee K. . ( 2013; ). Performance of the Vitek MS matrix-asisted laser desorption ionization time-of-flight mass spectrometry system for identification of Gram-positive cocci routinely isolated in clinical microbiology laboratories. . J Med Microbiol 62:, 1301–1306. [CrossRef] [PubMed]
    [Google Scholar]
  25. Parte A. C. . ( 2014; ). LPSN–list of prokaryotic names with standing in nomenclature. . Nucleic Acids Res 42: (D1), D613–D616. [CrossRef] [PubMed]
    [Google Scholar]
  26. Piñeiro-Vidal M. , Pazos F. , Santos Y. . ( 2008; ). Fatty acid analysis as a chemotaxonomic tool for taxonomic and epidemiological characterization of four fish pathogenic Tenacibaculum species. . Lett Appl Microbiol 46:, 548–554. [CrossRef] [PubMed]
    [Google Scholar]
  27. Posada D. . ( 2008; ). jModelTest: phylogenetic model averaging. . Mol Biol Evol 25:, 1253–1256. [CrossRef] [PubMed]
    [Google Scholar]
  28. Pot B. , Vandamme P. , Kersters K. . ( 1994; ). Analysis of electrophoretic whole-organism protein fingerprints. . In Modern Microbial Methods. Chemical Methods in Prokaryotic Systematics, pp. 493–521. Edited by Goodfellow M. , O’Donnell A. G. . . Chichester:: Wiley;.
    [Google Scholar]
  29. Poyart C. , Quesne G. , Coulon S. , Berche P. , Trieu-Cuot P. . ( 1998; ). Identification of streptococci to species level by sequencing the gene encoding the manganese-dependent superoxide dismutase. . J Clin Microbiol 36:, 41–47.[PubMed]
    [Google Scholar]
  30. Raverty, S. A., Gaydos, J. K., Nielsen, O. & Ross, P. (2004). Pathologic and clinical implications of Streptococcus phocae isolated from pinnipeds along coastal Washington state, British Columbia, and Arctic Canada. In Abstracts of the 35th Annual Conference of the International Association of Aquatic Animal Medicine, Galveston, TX, April 2004.
  31. Romalde J. L. , Ravelo C. , Valdés I. , Magariños B. , de la Fuente E. , Martín C. S. , Avendaño-Herrera R. , Toranzo A. E. . ( 2008; ). Streptococcus phocae, an emerging pathogen for salmonid culture. . Vet Microbiol 130:, 198–207. [CrossRef] [PubMed]
    [Google Scholar]
  32. Rosselló-Mora R. , Amann R. . ( 2001; ). The species concept for prokaryotes. . FEMS Microbiol Rev 25:, 39–67. [CrossRef] [PubMed]
    [Google Scholar]
  33. Sasser M. . ( 1990; ). Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Technical Note 101. . Newark, DE:: MIDI Inc;.
  34. Skaar I. , Gaustad P. , Tønjum T. , Holm B. , Stenwig H. . ( 1994; ). Streptococcus phocae sp. nov., a new species isolated from clinical specimens from seals. . Int J Syst Bacteriol 44:, 646–650. [CrossRef] [PubMed]
    [Google Scholar]
  35. Stackebrandt E. , Frederiksen W. , Garrity G. M. , Grimont P. A. D. , Kämpfer P. , Maiden M. C. J. , Nesme X. , Rosselló-Mora R. , Swings J. . & other authors ( 2002; ). Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. . Int J Syst Evol Microbiol 52:, 1043–1047. [CrossRef] [PubMed]
    [Google Scholar]
  36. Tamura K. , Dudley J. , Nei M. , Kumar S. . ( 2007; ). mega4: molecular evolutionary genetics analysis (mega) software version 4.0. . Mol Biol Evol 24:, 1596–1599. [CrossRef] [PubMed]
    [Google Scholar]
  37. Valdés I. , Jaureguiberry B. , Romalde J. L. , Toranzo A. E. , Magariños B. , Avendaño-Herrera R. . ( 2009; ). Genetic characterization of Streptococcus phocae strains isolated from Atlantic salmon, Salmo salar L., in Chile. . J Fish Dis 32:, 351–358. [CrossRef] [PubMed]
    [Google Scholar]
  38. Vandamme P. , Devriese L. A. , Pot B. , Kersters K. , Melin P. . ( 1997; ). Streptococcus difficile is a nonhemolytic group B, type Ib Streptococcus . . Int J Syst Bacteriol 47:, 81–85. [CrossRef] [PubMed]
    [Google Scholar]
  39. Vossen A. , Abdulmawjood A. , Lämmler C. , Weiss R. , Siebert U. . ( 2004; ). Identification and molecular characterization of beta-hemolytic streptococci isolated from harbor seals (Phoca vitulina) and grey seals (Halichoerus grypus) of the German North and Baltic Seas. . J Clin Microbiol 42:, 469–473. [CrossRef] [PubMed]
    [Google Scholar]
  40. Wang J. , Zhou N. , Xu B. , Hao H. , Kang L. , Zheng Y. , Jiang Y. , Jiang H. . ( 2012; ). Identification and cluster analysis of Streptococcus pyogenes by MALDI-TOF mass spectrometry. . PLoS ONE 7:, e47152. [CrossRef] [PubMed]
    [Google Scholar]
  41. Ziemke F. , Höfle M. G. , Lalucat J. , Rosselló-Mora R. . ( 1998; ). Reclassification of Shewanella putrefaciens Owen’s genomic group II as Shewanella baltica sp. nov.. Int J Syst Bacteriol 48:, 179–186. [CrossRef] [PubMed]
    [Google Scholar]
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