sp. nov., an anaerobic Gram-negative coccus isolated from the oral cavity of Japanese children Free

Abstract

Two strains of previously unknown Gram-negative cocci, T1-7 and S6-16, were isolated from the oral cavity of healthy Japanese children. The two strains showed atypical phenotypic characteristics of members of the genus , including catalase production. Sequencing of their 16S rRNA genes confirmed that they belong to genus . Under anaerobic conditions, the two strains produced acetic acid and propionic acid as metabolic end-products in a trypticase–yeast extract–haemin medium containing 1 % (w/v) glucose, 1 % (w/v) fructose and 1 % (v/v) sodium lactate. Comparative analysis of the 16S rRNA, , and gene sequences revealed that the two strains are phylogenetically homogeneous and comprise a distinct, novel lineage within the genus . The sequences from the two strains shared the highest similarity, at 99.9, 95.8, 96.9 and 96.7 %, using the partial 16S rRNA, , and gene sequences, respectively, with the type strains of the two most closely related species, ATCC 17748 and JCM 31738. Furthermore, strain T1-7 shared the highest average nucleotide identity (ANI) value (94.06 %) with type strain of the most closely related species, . At the same time, strain T1-7 showed the highest digital DNA–DNA hybridization (dDDH) value (55.5 %) with the type strain of . The two strains reported in this study were distinguished from the previously reported species from the genus based on catalase production, partial , and sequences, average ANI and dDDH values. Based on these observations, the two strains represent a novel species, for which the name sp. nov. is proposed. The type strain is T1-7 (JCM 33966=CCUG 74597).

Funding
This study was supported by the:
  • Kato Memorial Bioscience Foundation
    • Principle Award Recipient: IzumiMashima
  • Yakult Bio-Science Foundation
    • Principle Award Recipient: IzumiMashima
  • Japan Society for the Promotion of Science (Award 19K18975)
    • Principle Award Recipient: IzumiMashima
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004583
2020-12-02
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/71/1/ijsem004583.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004583&mimeType=html&fmt=ahah

References

  1. Parte AC. LPSN (List of Prokaryotic Names with Standing Nomenclature); 2020
  2. Mays TD, Holdeman LV, Moore WEC, Rogosa M, Johnson JL. Taxonomy of the genus Veillonella Prevot. Int J Syst Bacteriol 1982; 32:28–36 [View Article]
    [Google Scholar]
  3. Rogosa M. The genus Veillonella IV. serological groupings, and genus and species Emendations. J Bacteriol 1965; 90:704–709 [View Article][PubMed]
    [Google Scholar]
  4. Jumas-Bilak E, Carlier JP, Jean-Pierre H, Teyssier C, Gay B et al. Veillonella montpellierensis sp. nov., a novel, anaerobic, Gram-negative coccus isolated from human clinical samples. Int J Syst Evol Microbiol 2004; 54:1311–1316 [View Article][PubMed]
    [Google Scholar]
  5. Byun R, Carlier JP, Jacques NA, Marchandin H, Hunter N. Veillonella denticariosi sp. nov., isolated from human carious dentine. Int J Syst Evol Microbiol 2007; 57:2844–2848 [View Article][PubMed]
    [Google Scholar]
  6. Arif N, Do T, Byun R, Sheehy E, Clark D et al. Veillonella rogosae sp. nov., an anaerobic, Gram-negative coccus isolated from dental plaque. Int J Syst Evol Microbiol 2008; 58:581–584 [View Article][PubMed]
    [Google Scholar]
  7. Kraatz M, Taras D. Veillonella magna sp. nov., isolated from the jejunal mucosa of a healthy pig, and emended description of Veillonella ratti . Int J Syst Evol Microbiol 2008; 58:2755–2761 [View Article][PubMed]
    [Google Scholar]
  8. Mashima I, Kamaguchi A, Miyakawa H, Nakazawa F. Veillonella tobetsuensis sp. nov., an anaerobic, gram-negative coccus isolated from human tongue biofilms. Int J Syst Evol Microbiol 2013; 63:1443–1449 [View Article][PubMed]
    [Google Scholar]
  9. Aujoulat F, Bouvet P, Jumas-Bilak E, Jean-Pierre H, Marchandin H. Veillonella seminalis sp. nov., a novel anaerobic Gram-stain-negative coccus from human clinical samples, and emended description of the genus Veillonella . Int J Syst Evol Microbiol 2014; 64:3526–3531 [View Article][PubMed]
    [Google Scholar]
  10. Mashima I, Liao YC, Miyakawa H, Theodorea CF, Thawboon B et al. Veillonella infantium sp. nov., an anaerobic, Gram-stain-negative coccus isolated from tongue biofilm of a Thai child. Int J Syst Evol Microbiol 2018; 68:1101–1106 [View Article][PubMed]
    [Google Scholar]
  11. Carlier JP. Veillonella. Bergey’s Manual of Systematics of Archaea and Bacteria 2015 pp 1–11
    [Google Scholar]
  12. Delwiche EA, Pestka JJ, Tortorello ML. The veillonellae: gram-negative cocci with a unique physiology. Annu Rev Microbiol 1985; 39:175–193 [View Article][PubMed]
    [Google Scholar]
  13. Foubert EL, Douglas HC. Studies on the anaerobic micrococci. Ⅱ. The fermentation of lactate by Micrococcus lactilyticus. J Bacteriol 1948; 56:35–36
    [Google Scholar]
  14. Rogosa M. Anaerobic Gram-negative cocci. In Krieg NR, Holt JG. (editors) Bergey’s Manual of Systematic Bacteriology 1 Baltimore: Williams & Wilkins; 1984 pp 680–685
    [Google Scholar]
  15. Ng SK, Hamilton IR. Lactate metabolism by Veillonella parvula . J Bacteriol 1971; 105:999–1005 [View Article][PubMed]
    [Google Scholar]
  16. Scheiman J, Luber JM, Chavkin TA, MacDonald T, Tung A et al. Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism. Nat Med 2019; 25:1104–1109 [View Article][PubMed]
    [Google Scholar]
  17. Mashima I, Theodorea CF, Thaweboon B, Thaweboon S, Scannapieco FA et al. Exploring the salivary microbiome of children stratified by the oral hygiene index. PLoS One 2017; 12:e0185274 [View Article][PubMed]
    [Google Scholar]
  18. Mashima I, Theodorea CF, Thaweboon B, Thaweboon S, Vichayanrat T et al. Characterization of salivary microbiome in healthy Thai children. Asian Pac J Trop Med 2019; 12:163–169
    [Google Scholar]
  19. Mashima I, Kamaguchi A, Nakazawa F. The distribution and frequency of oral Veillonella spp. in the tongue biofilm of healthy young adults. Curr Microbiol 2011; 63:403–407 [View Article][PubMed]
    [Google Scholar]
  20. Mashima I, Fujita M, Nakatsuka Y, Kado T, Furuichi Y et al. The distribution and frequency of Veillonella spp. associated with chronic periodontal diseases. Int J Curr Microbiol Appl Sci 2015; 4:150–160
    [Google Scholar]
  21. Mashima I, Theodorea CF, Thaweboon B, Thaweboon S, Nakazawa F. Identification of Veillonella species in the tongue biofilm by using a novel one-step polymerase chain reaction method. PLoS One 2016; 11:e0157516 [View Article][PubMed]
    [Google Scholar]
  22. Theodorea CF, Mashima I, Thaweboon B, Thaweboon S, Nakazawa F. Molecular detection of oral Veillonella species in the saliva of children with different oral hygiene statuses. Int J Curr Microbiol Appl Sci 2017; 6:449–461
    [Google Scholar]
  23. Djais AA, Theodorea CF, Mashima I, Otomo M, Saitoh M et al. Identification and phylogenetic analysis of oral Veillonella species isolated from the saliva of Japanese children. F1000Res 2019; 8:616 [View Article][PubMed]
    [Google Scholar]
  24. Theodorea CF, Djais AA, Mashima I, Otomo M, Saitoh M et al. Phylogenetic study of oral Veillonella isolates from saliva of children in Hokkaido. Dent J Heal Sci Univ Hokkaido 2019; 38:37–46
    [Google Scholar]
  25. Mashima I, Miyoshi-Akiyama T, Tomida J, Kutsuna R, Washio J et al. Draft genome sequences of two Veillonella tobetsuensis clinical isolates from intraoperative bronchial fluids of elderly patients with pulmonary carcinoma. Microbiol Resour Announc 2019; 8:e00397–19 [View Article][PubMed]
    [Google Scholar]
  26. Sato T, Sato M, Matsuyama J, Hoshino E. PCR-restriction fragment length polymorphism analysis of genes coding for 16S rRNA in Veillonella spp. Int J Syst Bacteriol 1997; 47:1268–1270 [View Article][PubMed]
    [Google Scholar]
  27. Marchandin H, Teyssier C, Siméon de Buochberg M, Jean-Pierre H, Carriere C et al. Intra-chromosomal heterogeneity between the four 16S rRNA gene copies in the genus Veillonella: implications for phylogeny and taxonomy. Microbiology 2003; 149:1493–1501 [View Article][PubMed]
    [Google Scholar]
  28. Marchandin H, Teyssier C, Jumas-Bilak E, Robert M, Artigues AC et al. Molecular identification of the first human isolate belonging to the Veillonella ratti-Veillonella criceti group based on 16S rDNA and dnaK gene sequencing. Res Microbiol 2005; 156:603–607 [View Article][PubMed]
    [Google Scholar]
  29. Michon AL, Aujoulat F, Roudière L, Soulier O, Zorgniotti I et al. Intragenomic and intraspecific heterogeneity in rrs may surpass interspecific variability in a natural population of Veillonella . Microbiology 2010; 156:2080–2091 [View Article][PubMed]
    [Google Scholar]
  30. Rogosa M. A selective medium for the isolation and enumeration of the Veillonella from the oral cavity. J Bacteriol 1956; 72:533–536 [View Article][PubMed]
    [Google Scholar]
  31. Carlier JP, Marchandin H, Jumas-Bilak E, Lorin V, Henry C et al. Anaeroglobus geminatus gen. nov., sp. nov., a novel member of the family Veillonellaceae . Int J Syst Evol Microbiol 2002; 52:983–986 [View Article][PubMed]
    [Google Scholar]
  32. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN et al. Bacterial diversity in human subgingival plaque. J Bacteriol 2001; 183:3770–3783 [View Article][PubMed]
    [Google Scholar]
  33. Kim M, Oh H-S, Park S-C, 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]
  34. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article][PubMed]
    [Google Scholar]
  35. Olsen GJ, Matsuda H, Hagstrom R, Overbeek R. fastDNAmL: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput Appl Biosci 1994; 10:41–48 [View Article][PubMed]
    [Google Scholar]
  36. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article][PubMed]
    [Google Scholar]
  37. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 2006; 33:152–155
    [Google Scholar]
  38. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014; 12:635–645 [View Article][PubMed]
    [Google Scholar]
  39. Marmur J. A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 1961; 3:208–218 [View Article]
    [Google Scholar]
  40. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article][PubMed]
    [Google Scholar]
  41. Yoon SH, 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]
  42. Figueras MJ, Beaz-Hidalgo R, Hossain MJ, Liles MR. Taxonomic affiliation of new genomes should be verified using average nucleotide identity and multilocus phylogenetic analysis. Genome Announc 2014; 2:e00927–14 [View Article][PubMed]
    [Google Scholar]
  43. Lee I, Ouk Kim Y, Park S-C, Chun J, Kim YO, Chum 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]
  44. Ciufo S, Kannan S, Sharma S, Badretdin A, Clark K et al. Using average nucleotide identity to improve taxonomic assignments in prokaryotic genomes at the NCBI. Int J Syst Evol Microbiol 2018; 68:2386–2392 [View Article][PubMed]
    [Google Scholar]
  45. Meier-Kolthoff JP, Klenk HP, Goker M. Taxonomic use of DNA G+C content and DNA-DNA hybridization in the genomic age. Int J Syst Evol Microbiol 2014; 64:352–356 [View Article][PubMed]
    [Google Scholar]
  46. Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  47. Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST. Bergey’s Manual of Determinative Bacteriology, 9th edn. Baltimore: Williams & Wilkins; 1994
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004583
Loading
/content/journal/ijsem/10.1099/ijsem.0.004583
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed