1887

Abstract

One novel strain (SQ9-PEA) and two novel strains (SQ8-PEA and GRT3) were isolated from faeces of a wild eastern grey squirrel. The strains were non-spore-forming, non-motile Gram-positive cocci, facultative anaerobes. The genomes for these strains were sequenced. The 16S rRNA gene and core-genome-based phylogenetic analyses showed that strain SQ9-PEA was closely related to , strain SQ8-PEA to and , and strain GRT3 to , and . Average nucleotide identity and pairwise digital DNA–DNA hybridization values calculated for these novel strains compared to type strain genomes of phylogenetically related species within the genera and clearly revealed that strain SQ9-PEA represents a novel species of the genus and strains SQ8-PEA and GRT3 represent two novel species of the genus . Phenotypical features of these novel type strains differed from the features of the type strains of other phylogenetically related species. MALDI-TOF mass spectrometry supported identification of these novel species. Based on these data, we propose one novel species of the genus , for which the name sp. nov. with the type strain SQ9-PEA (=DSM 114656=CCUG 76426=NCTC 14727) is proposed, and two novel species of the genus , for which the names sp. nov. with the type strain SQ8-PEA (=DSM 114685=CCUG 76423=NCTC 14723) and sp. nov. with the type strain GRT3 (=DSM 114696=CCUG 76427=NCTC 14722) are proposed. The genome G+C contents are 38.29, 36.49 and 37.26 mol% and complete draft genome sizes are 1 692 266, 2 371 088 and 2 237 001 bp for strains SQ9-PEA, SQ8-PEA and GRT3, respectively.

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/content/journal/ijsem/10.1099/ijsem.0.006015
2023-08-14
2024-05-09
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References

  1. Whiley RA, Hardie JM. Streptococcus. In Whitman WB. eds Bergey’s Manual of Systematics of Archaea and Bacteria John Wiley & Sons, Inc; 2015
    [Google Scholar]
  2. Schleifer KH, Bell JA. Staphylococcus. In Whitman WB. eds Bergey’s Manual of Systematics of Archaea and Bacteria John Wiley & Sons, Inc; 2015
    [Google Scholar]
  3. Fountain K, Blackett T, Butler H, Carchedi C, Schilling A-K et al. Fatal exudative dermatitis in island populations of red squirrels (Sciurus vulgaris): spillover of a virulent Staphylococcus aureus clone (ST49) from reservoir hosts. Microb Genom 2021; 7:000565 [View Article] [PubMed]
    [Google Scholar]
  4. Garcia-Alvarez L, Dawson S, Cookson B, Hawkey P. Working across the veterinary and human health sectors. J Antimicrob Chemother 2012; 67 Suppl 1:i37–49 [View Article] [PubMed]
    [Google Scholar]
  5. White FH, Hoff GL, Bigler WJ, Buff E. A microbiologic study of the urban gray squirrel. J Am Vet Med Assoc 1975; 167:603–604 [PubMed]
    [Google Scholar]
  6. Simpson VR, Davison NJ, Kearns AM, Pichon B, Hudson LO et al. Association of a lukM-positive clone of Staphylococcus aureus with fatal exudative dermatitis in red squirrels (Sciurus vulgaris). Vet Microbiol 2013; 162:987–991 [View Article] [PubMed]
    [Google Scholar]
  7. Pauls RW. Body temperature dynamics of the red squirrel (Tamiasciurus hudsonicus): adaptations for energy conservation. Can J Zool 1979; 57:1349–1354 [View Article] [PubMed]
    [Google Scholar]
  8. Muchlinski AE, Baldwin BC, Padick DA, Lee BY, Salguero HS et al. California ground squirrel body temperature regulation patterns measured in the laboratory and in the natural environment. Comp Biochem Physiol A Mol Integr Physiol 1998; 120:365–372 [View Article] [PubMed]
    [Google Scholar]
  9. Lee BY, Padick DA, Muchlinski AE. Stress fever magnitude in laboratory-maintained California ground squirrels varies with season. Comp Biochem Physiol A Mol Integr Physiol 2000; 125:325–330 [View Article] [PubMed]
    [Google Scholar]
  10. Sutton JAF, Carnell OT, Lafage L, Gray J, Biboy J et al. Staphylococcus aureus cell wall structure and dynamics during host-pathogen interaction. PLoS Pathog 2021; 17:e1009468 [View Article] [PubMed]
    [Google Scholar]
  11. Su H-N, Li K, Zhao L-S, Yuan X-X, Zhang M-Y et al. Structural visualization of septum formation in Staphylococcus warneri using atomic force microscopy. J Bacteriol 2020; 202:e00294–20 [View Article]
    [Google Scholar]
  12. 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]
  13. Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA et al. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 2008; 74:2461–2470 [View Article] [PubMed]
    [Google Scholar]
  14. McGinnis S, Madden TL. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 2004; 32:W20–5 [View Article] [PubMed]
    [Google Scholar]
  15. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article] [PubMed]
    [Google Scholar]
  16. 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]
  17. Volokhov DV, Simonyan V, Davidson MK, Chizhikov VE. RNA polymerase beta subunit (rpoB) gene and the 16S-23S rRNA intergenic transcribed spacer region (ITS) as complementary molecular markers in addition to the 16S rRNA gene for phylogenetic analysis and identification of the species of the family Mycoplasmataceae. Mol Phylogenet Evol 2012; 62:515–528 [View Article] [PubMed]
    [Google Scholar]
  18. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 2006; 33:152–155
    [Google Scholar]
  19. 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]
  20. Morales-Covarrubias MS, Del Carmen Bolan-Mejía M, Vela Alonso AI, Fernandez-Garayzabal JF, Gomez-Gil B. Streptococcus penaeicida sp. nov., isolated from a diseased farmed Pacific white shrimp (Penaeus vannamei). Int J Syst Evol Microbiol 2018; 68:1490–1495 [View Article] [PubMed]
    [Google Scholar]
  21. Huch M, De Bruyne K, Cleenwerck I, Bub A, Cho G-S et al. Streptococcus rubneri sp. nov., isolated from the human throat. Int J Syst Evol Microbiol 2013; 63:4026–4032 [View Article] [PubMed]
    [Google Scholar]
  22. Volokhov DV, Zagorodnyaya TA, Shen Z, Blom J, Furtak VA et al. Streptococcus vicugnae sp. nov., isolated from faeces of alpacas (Vicugna pacos) and cattle (Bos taurus) Streptococcus zalophi sp. nov., and Streptococcus pacificus sp. nov. Int J Syst Evol Microbiol 2021; 71:
    [Google Scholar]
  23. Taponen S, Supré K, Piessens V, Van Coillie E, De Vliegher S et al. Staphylococcus agnetis sp. nov., a coagulase-variable species from bovine subclinical and mild clinical mastitis. Int J Syst Evol Microbiol 2012; 62:61–65 [View Article] [PubMed]
    [Google Scholar]
  24. Riesen A, Perreten V. Staphylococcus rostri sp. nov., a haemolytic bacterium isolated from the noses of healthy pigs. Int J Syst Evol Microbiol 2010; 60:2042–2047 [View Article] [PubMed]
    [Google Scholar]
  25. MacFadyen AC, Leroy S, Harrison EM, Parkhill J, Holmes MA et al. Staphylococcus pseudoxylosus sp. nov., isolated from bovine mastitis. Int J Syst Evol Microbiol 2019; 69:2208–2213 [View Article] [PubMed]
    [Google Scholar]
  26. Lamers RP, Muthukrishnan G, Castoe TA, Tafur S, Cole AM et al. Phylogenetic relationships among Staphylococcus species and refinement of cluster groups based on multilocus data. BMC Evol Biol 2012; 12:171 [View Article] [PubMed]
    [Google Scholar]
  27. Poyart C, Quesne G, Boumaila C, Trieu-Cuot P. Rapid and accurate species-level identification of coagulase-negative staphylococci by using the sodA gene as a target. J Clin Microbiol 2001; 39:4296–4301 [View Article] [PubMed]
    [Google Scholar]
  28. Ghebremedhin B, Layer F, König W, König B. Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. J Clin Microbiol 2008; 46:1019–1025 [View Article] [PubMed]
    [Google Scholar]
  29. Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics 2020; 70:e102 [View Article] [PubMed]
    [Google Scholar]
  30. Simonyan V, Chumakov K, Dingerdissen H, Faison W, Goldweber S et al. High-performance integrated virtual environment (HIVE): a robust infrastructure for next-generation sequence data analysis. Database 2016; 2016:baw022 [View Article]
    [Google Scholar]
  31. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
    [Google Scholar]
  32. Dieckmann MA, Beyvers S, Nkouamedjo-Fankep RC, Hanel PHG, Jelonek L et al. EDGAR3.0: comparative genomics and phylogenomics on a scalable infrastructure. Nucleic Acids Res 2021; 49:W185–W192 [View Article] [PubMed]
    [Google Scholar]
  33. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article] [PubMed]
    [Google Scholar]
  34. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 2009; 106:19126–19131 [View Article] [PubMed]
    [Google Scholar]
  35. Konstantinidis KT, Tiedje JM. Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 2007; 10:504–509 [View Article] [PubMed]
    [Google Scholar]
  36. Konstantinidis KT, Ramette A, Tiedje JM. The bacterial species definition in the genomic era. Philos Trans R Soc Lond B Biol Sci 2006; 361:1929–1940 [View Article] [PubMed]
    [Google Scholar]
  37. 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]
  38. Medlar AJ, Törönen P, Holm L. AAI-profiler: fast proteome-wide exploratory analysis reveals taxonomic identity, misclassification and contamination. Nucleic Acids Res 2018; 46:W479–W485 [View Article] [PubMed]
    [Google Scholar]
  39. Konstantinidis KT, Tiedje JM. Towards a genome-based taxonomy for prokaryotes. J Bacteriol 2005; 187:6258–6264 [View Article] [PubMed]
    [Google Scholar]
  40. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe Magazine 2014; 9:111–118 [View Article]
    [Google Scholar]
  41. Palmer M, Venter SN, McTaggart AR, Coetzee MPA, Van Wyk S et al. The synergistic effect of concatenation in phylogenomics: the case in Pantoea. PeerJ 2019; 7:e6698 [View Article] [PubMed]
    [Google Scholar]
  42. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  43. Price MN, Dehal PS, Arkin AP. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
    [Google Scholar]
  44. Shimodaira H, Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 1999; 16:1114–1116 [View Article]
    [Google Scholar]
  45. Patel S, Gupta RS. Robust demarcation of fourteen different species groups within the genus Streptococcus based on genome-based phylogenies and molecular signatures. Infect Genet Evol 2018; 66:130–151 [View Article] [PubMed]
    [Google Scholar]
  46. Xu L, Dong Z, Fang L, Luo Y, Wei Z et al. OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 2019; 47:W52–W58 [View Article] [PubMed]
    [Google Scholar]
  47. Blom J, Kreis J, Spänig S, Juhre T, Bertelli C et al. EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic Acids Res 2016; 44:W22–8 [View Article] [PubMed]
    [Google Scholar]
  48. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA et al. The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 2013; 57:3348–3357 [View Article] [PubMed]
    [Google Scholar]
  49. Liu B, Zheng D, Zhou S, Chen L, Yang J. VFDB 2022: a general classification scheme for bacterial virulence factors. Nucleic Acids Res 2022; 50:D912–D917 [View Article] [PubMed]
    [Google Scholar]
  50. Trülzsch K, Grabein B, Schumann P, Mellmann A, Antonenka U et al. Staphylococcus pettenkoferi sp. nov., a novel coagulase-negative staphylococcal species isolated from human clinical specimens. Int J Syst Evol Microbiol 2007; 57:1543–1548 [View Article] [PubMed]
    [Google Scholar]
  51. Devriese LA, KILPPER-BaLZ R, Schleifer KH. Notes: Streptococcus hyointestinalis sp. nov. from the gut of swine. Int J Syst Bacteriol 1988; 38:440–441 [View Article]
    [Google Scholar]
  52. Tappe D, Pukall R, Schumann P, Gronow S, Spiliotis M et al. Streptococcus merionis sp. nov., isolated from Mongolian jirds (Meriones unguiculatus). Int J Syst Evol Microbiol 2009; 59: [View Article]
    [Google Scholar]
  53. Baker CN, Stocker SA, Culver DH, Thornsberry C. Comparison of the E test to agar dilution, broth microdilution, and agar diffusion susceptibility testing techniques by using a special challenge set of bacteria. J Clin Microbiol 1991; 29:533–538 [View Article] [PubMed]
    [Google Scholar]
  54. Dubois D, Leyssene D, Chacornac JP, Kostrzewa M, Schmit PO et al. Identification of a variety of Staphylococcus species by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol 2010; 48:941–945 [View Article] [PubMed]
    [Google Scholar]
  55. Pérez-Sancho M, Vela AI, García-Seco T, González S, Domínguez L et al. Usefulness of MALDI-TOF MS as a diagnostic tool for the identification of Streptococcus species recovered from clinical specimens of pigs. PLoS One 2017; 12:e0170784 [View Article] [PubMed]
    [Google Scholar]
  56. Rau J, Eisenberg T, Male A, Wind C, Lasch P et al. MALDI-UP – an Internet platform for the exchange of MALDI-TOF mass spectra. Aspect Food Control Anim Health 2016; 1:1–17
    [Google Scholar]
  57. Volokhov DV, Amselle M, Bodeis-Jones S, Delmonte P, Zhang S et al. Neisseria zalophi sp. nov., isolated from oral cavity of California sea lions (Zalophus californianus). Arch Microbiol 2018; 200:819–828 [View Article] [PubMed]
    [Google Scholar]
  58. Whittaker P, Keys CE, Brown EW, Fry FS. Differentiation of Enterobacter sakazakii from closely related Enterobacter and Citrobacter species using fatty acid profiles. J Agric Food Chem 2007; 55:4617–4623 [View Article] [PubMed]
    [Google Scholar]
  59. Delmonte P, Kia A-RF, Hu Q, Rader JI. Review of methods for preparation and gas chromatographic separation of trans and cis reference fatty acids. J AOAC Int 2009; 92:1310–1326 [PubMed]
    [Google Scholar]
  60. Delmonte P, Fardin-Kia AR, Rader JI. Separation of fatty acid methyl esters by GC-online hydrogenation × GC. Anal Chem 2013; 85:1517–1524 [View Article] [PubMed]
    [Google Scholar]
  61. Durham DR, Kloos WE. Comparative study of the total cellular fatty acids of Staphylococcus species of human origin. Int J Syst Bacteriol 1978; 28:223–228 [View Article]
    [Google Scholar]
  62. Nováková D, Pantůček R, Hubálek Z, Falsen E, Busse H-J et al. Staphylococcus microti sp. nov., isolated from the common vole (Microtus arvalis). Int J Syst Evol Microbiol 2010; 60:566–573 [View Article] [PubMed]
    [Google Scholar]
  63. Hájek V, Ludwig W, Schleifer KH, Springer N, Zitzelsberger W et al. Staphylococcus muscae, a new species isolated from flies. Int J Syst Bacteriol 1992; 42:97–101 [View Article] [PubMed]
    [Google Scholar]
  64. Heß S, Gallert C. Staphylococcus argensis sp. nov., a novel staphylococcal species isolated from an aquatic environment. Int J Syst Evol Microbiol 2015; 65:2661–2665 [View Article] [PubMed]
    [Google Scholar]
  65. Kämpfer P, Glaeser SP. Prokaryotic taxonomy in the sequencing era–the polyphasic approach revisited. Environ Microbiol 2012; 14:291–317 [View Article] [PubMed]
    [Google Scholar]
  66. Vitetta L, Llewellyn H, Oldfield D. Gut dysbiosis and the intestinal microbiome: Streptococcus thermophilus a key probiotic for reducing uremia. Microorganisms 2019; 7:228 [View Article] [PubMed]
    [Google Scholar]
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