sp. nov., a coagulase-negative species from bovine milk Open Access

Abstract

A novel type strain, designated SDB 2975 (=CECT 9737=DSM 105892), of the novel species sp. nov. isolated from bovine milk is described. The novel species belongs to the genus and showed resistance to tetracycline and was oxidase- and coagulase-negative, catalase-positive, and Gram-stain-positive. Phylogenetic relationships of SDB 2975 to other staphylococcal species were inferred from 16S rRNA gene and whole-genome-based phylogenetic reconstruction. The 16S rRNA gene comparisons showed that the strain is closely related to (99.73 %), (99.66 %), (99.59 %) and (98.03 %). Average nucleotide identity (ANI) values between SDB 2975 and its closely related species were 83.96, 94.5, 84.03 and 78.09 %, respectively, and digital DNA–DNA hybridization (dDDH) values were 27.70, 58.02, 27.70 and 22.00 %, respectively. The genome of SDB 2975 was sequenced with PacBio and Illumina technologies and is 2 691 850 bp long, has a G+C content of 36.6 mol% and contains 2678 genes and 80 RNAs, including six copies of each5S rRNA, 16S rRNA and 23S rRNA genes. Biochemical profiling and a newly developed PCR assay enabled differentiation of SDB 2975 and three other SDB strains from its closest staphylococcal species. Differentiation was also achieved by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF). Genes unique to were identified and a PCR-based assay was developed to differentiate from other staphylococcal species. In conclusion, the results of phylogenetic analysis along with the ANI values <95 %, and dDDH values <70 % from closely related species along with the phenotypic and biochemical characteristics and specific MALDI-TOF profiles demonstrated that SDB 2975 represents a novel species within the genus , named sp. nov. (SDB 2975=CECT 9737=DSM 105892).

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2019-08-01
2024-03-28
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References

  1. De Visscher A, Piepers S, Haesebrouck F, de Vliegher S. Intramammary infection with coagulase-negative staphylococci at parturition: species-specific prevalence, risk factors, and effect on udder health. J Dairy Sci 2016; 99:6457–6469 [View Article][PubMed]
    [Google Scholar]
  2. Condas LAZ, De Buck J, Nobrega DB, Carson DA, Naushad S et al. Prevalence of non-aureus staphylococci species causing intramammary infections in Canadian dairy herds. J Dairy Sci 2017; 100:5592–5612 [View Article][PubMed]
    [Google Scholar]
  3. Vanderhaeghen W, Piepers S, Leroy F, van Coillie E, Haesebrouck F et al. Invited review: effect, persistence, and virulence of coagulase-negative Staphylococcus species associated with ruminant udder health. J Dairy Sci 2014; 97:5275–5293 [View Article][PubMed]
    [Google Scholar]
  4. De Vliegher S, Fox LK, Piepers S, McDougall S, Barkema HW. Invited review: mastitis in dairy heifers: nature of the disease, potential impact, prevention, and control. J Dairy Sci 2012; 95:1025–1040 [View Article][PubMed]
    [Google Scholar]
  5. Rosenbach FJ. Microorganismen bei den wund-infections-krankheiten des menschen. J.F. Bergmann, Wiesbaden 1884; 122:1
    [Google Scholar]
  6. Nobrega DB, Naushad S, Naqvi SA, Condas LAZ, Saini V et al. Prevalence and genetic basis of antimicrobial resistance in Non-aureus Staphylococci isolated from Canadian dairy herds. Front Microbiol 2018; 9:256 [View Article][PubMed]
    [Google Scholar]
  7. Naushad S, Barkema HW, Luby C, Condas LA, Nobrega DB et al. Comprehensive phylogenetic analysis of bovine non-aureus Staphylococci species based on whole-genome sequencing. Front Microbiol 2016; 7:7 [View Article][PubMed]
    [Google Scholar]
  8. Naushad S, Naqvi SA, Nobrega D, Luby C, Kastelic JP et al. Comprehensive virulence gene profiling of bovine non-aureus Staphylococci based on whole-genome sequencing data. mSystems 2019; 4:e0009818 [View Article][PubMed]
    [Google Scholar]
  9. Kloos WE. Natural populations of the genus Staphylococcus . Annu Rev Microbiol 1980; 34:559–592 [View Article][PubMed]
    [Google Scholar]
  10. Kloos WE, Ballard DN, George CG, Webster JA, Hubner RJ et al. Delimiting the genus Staphylococcus through description of Macrococcus caseolyticus gen. nov., comb. nov. and Macrococcus equipercicus sp. nov., and Macrococcus bovicus sp. no. and Macrococcus carouselicus sp. nov. Int J Syst Bacteriol 1998; 48 Pt 3:859–877 [View Article][PubMed]
    [Google Scholar]
  11. Kloos WE, George CG, Olgiate JS, van Pelt L, Mckinnon ML et al. Staphylococcus hominis subsp. novobiosepticus subsp. nov., a novel trehalose- and N-acetyl-D-glucosamine-negative, novobiocin- and multiple-antibiotic-resistant subspecies isolated from human blood cultures. Int J Syst Bacteriol 1998; 48 Pt 3:799–812 [View Article][PubMed]
    [Google Scholar]
  12. Bannerman TL, Kloos WE. Staphylococcus capitis subsp. ureolyticus subsp. nov. from human skin. Int J Syst Bacteriol 1991; 41:144–147 [View Article][PubMed]
    [Google Scholar]
  13. Pantůček R, Sedláček I, Indráková A, Vrbovská V, Mašlaňová I et al. Staphylococcus edaphicus sp. nov., isolated in Antarctica, Harbors the mecC gene and genomic Islands with a suspected role in adaptation to extreme environments. Appl Environ Microbiol 2018; 84:e0174617 [View Article][PubMed]
    [Google Scholar]
  14. Nováková D, Pantůcek R, Hubálek Z, Falsen E, Busse HJ 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]
  15. Tong SY, Schaumburg F, Ellington MJ, Corander J, Pichon B et al. Novel staphylococcal species that form part of a Staphylococcus aureus-related complex: the non-pigmented Staphylococcus argenteus sp. nov. and the non-human primate-associated Staphylococcus schweitzeri sp. nov. Int J Syst Evol Microbiol 2015; 65:15–22 [View Article][PubMed]
    [Google Scholar]
  16. Åvall-Jääskeläinen S, Taponen S, Kant R, Paulin L, Blom J et al. Comparative genome analysis of 24 bovine-associated Staphylococcus isolates with special focus on the putative virulence genes. PeerJ 2018; 6:e4560 [View Article][PubMed]
    [Google Scholar]
  17. Freney J, Kloos WE, Hajek V, Webster JA, Bes M et al. Recommended minimal standards for description of new staphylococcal species. Subcommittee on the taxonomy of staphylococci and streptococci of the International Committee on Systematic Bacteriology. Int J Syst Bacteriol 1999; 49 Pt 2:489–502 [View Article][PubMed]
    [Google Scholar]
  18. Svec P, Vancanneyt M, Sedlácek I, Engelbeen K, Stetina V et al. Reclassification of Staphylococcus pulvereri Zakrzewska-Czerwinska et al. 1995 as a later synonym of Staphylococcus vitulinus Webster et al. 1994. Int J Syst Evol Microbiol 2004; 54:2213–2215 [View Article][PubMed]
    [Google Scholar]
  19. Švec P, Petráš P, Pantůček R, Doškař J, Sedláček I. High intraspecies heterogeneity within Staphylococcus sciuri and rejection of its classification into S. sciuri subsp. sciuri, S. sciuri subsp. carnaticus and S. sciuri subsp. rodentium . Int J Syst Evol Microbiol 2016; 66:5181–5186 [View Article][PubMed]
    [Google Scholar]
  20. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 2014; 64:316–324 [View Article][PubMed]
    [Google Scholar]
  21. Varghese NJ, Mukherjee S, Ivanova N, Konstantinidis KT, Mavrommatis K et al. Microbial species delineation using whole genome sequences. Nucleic Acids Res 2015; 43:6761–6771 [View Article][PubMed]
    [Google Scholar]
  22. Konstantinidis KT, Stackebrandt E. Defining taxonomic ranks. The Prokaryotes vol. 1 Springer; 2013 pp. 229–254
    [Google Scholar]
  23. 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]
  24. 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]
  25. Singhal N, Kumar M, Kanaujia PK, Virdi JS. MALDI-TOF mass spectrometry: an emerging technology for microbial identification and diagnosis. Front Microbiol 2015; 6:791 [View Article][PubMed]
    [Google Scholar]
  26. Nicholson AC, Gulvik CA, Whitney AM, Humrighouse BW, Graziano J et al. Revisiting the taxonomy of the genus Elizabethkingia using whole-genome sequencing, optical mapping, and MALDI-TOF, along with proposal of three novel Elizabethkingia species: Elizabethkingia bruuniana sp. nov., Elizabethkingia ursingii sp. nov., and Elizabethkingia occulta sp. nov. Antonie van Leeuwenhoek 2018; 111:55–72 [View Article][PubMed]
    [Google Scholar]
  27. 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]
  28. Rosselló-Mora R. DNA-DNA reassociation methods applied to microbial taxonomy and their critical evaluation. In Stackebrandt E. (editor) Molecular Identification, Systematics, and Population Structure of Prokaryotes Springer; 2006 pp. 23–50
    [Google Scholar]
  29. Peeters C, Meier-Kolthoff JP, Verheyde B, de Brandt E, Cooper VS et al. Phylogenomic study of Burkholderia glathei-like organisms, proposal of 13 novel Burkholderia species and emended descriptions of Burkholderia sordidicola, Burkholderia zhejiangensis and Burkholderia grimmiae . Front Microbiol 2016; 7:877 [View Article][PubMed]
    [Google Scholar]
  30. Huang CH, Liou JS, Lee AY, Tseng M, Miyashita M et al. Polyphasic characterization of a novel species in the Lactobacillus casei group from cow manure of Taiwan: Description of L. chiayiensis sp. nov. Syst Appl Microbiol 2018; 41:270–278 [View Article][PubMed]
    [Google Scholar]
  31. Lugli GA, Mangifesta M, Duranti S, Anzalone R, Milani C et al. Phylogenetic classification of six novel species belonging to the genus Bifidobacterium comprising Bifidobacterium anseris sp. nov., Bifidobacterium criceti sp. nov., Bifidobacterium imperatoris sp. nov., Bifidobacterium italicum sp. nov., Bifidobacterium margollesii sp. nov. and Bifidobacterium parmae sp. nov. Syst Appl Microbiol 2018; 41:173–183 [View Article][PubMed]
    [Google Scholar]
  32. Tindall BJ, Rosselló-Móra R, Busse HJ, Ludwig W, Kämpfer P. Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 2010; 60:249–266 [View Article][PubMed]
    [Google Scholar]
  33. Reyher KK, Dufour S, Barkema HW, des Côteaux L, Devries TJ et al. The National Cohort of Dairy Farms-a data collection platform for mastitis research in Canada. J Dairy Sci 2011; 94:1616–1626 [View Article][PubMed]
    [Google Scholar]
  34. Oren A. The phyla of prokaryotes - cultured and uncultured. In Oren A, Papke RT. (editors) Molecular Phylogeny of Microorganisms Norfolk, UK: Caister Academic Press; 2010 pp. 85–107
    [Google Scholar]
  35. Tindall BJ, Kämpfer P, Euzéby JP, Oren A. Valid publication of names of prokaryotes according to the rules of nomenclature: past history and current practice. Int J Syst Evol Microbiol 2006; 56:2715–2720 [View Article][PubMed]
    [Google Scholar]
  36. Ramasamy D, Mishra AK, Lagier JC, Padhmanabhan R, Rossi M et al. A polyphasic strategy incorporating genomic data for the taxonomic description of novel bacterial species. Int J Syst Evol Microbiol 2014; 64:384–391 [View Article][PubMed]
    [Google Scholar]
  37. 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]
  38. Oren A, Garrity GM. Then and now: a systematic review of the systematics of prokaryotes in the last 80 years. Antonie van Leeuwenhoek 2014; 106:43–56 [View Article][PubMed]
    [Google Scholar]
  39. Janda JM, Abbott SL. 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol 2007; 45:2761–2764 [View Article][PubMed]
    [Google Scholar]
  40. Naushad S, Adeolu M, Wong S, Sohail M, Schellhorn HE et al. A phylogenomic and molecular marker based taxonomic framework for the order Xanthomonadales: proposal to transfer the families Algiphilaceae and Solimonadaceae to the order Nevskiales ord. nov. and to create a new family within the order Xanthomonadales, the family Rhodanobacteraceae fam. nov., containing the genus Rhodanobacter and its closest relatives. Antonie van Leeuwenhoek 2015; 107:467–485 [View Article][PubMed]
    [Google Scholar]
  41. Naushad S, Adeolu M, Goel N, Khadka B, Al-Dahwi A et al. Phylogenomic and molecular demarcation of the core members of the polyphyletic pasteurellaceae genera actinobacillus, haemophilus, and pasteurella. Int J Genomics 2015; 2015:1–15 [View Article][PubMed]
    [Google Scholar]
  42. Adeolu M, Alnajar S, Naushad S, S Gupta R. Genome-based phylogeny and taxonomy of the 'Enterobacteriales': proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 2016; 66:5575–5599 [View Article][PubMed]
    [Google Scholar]
  43. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006; 22:1658–1659 [View Article][PubMed]
    [Google Scholar]
  44. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 2012; 28:3150–3152 [View Article][PubMed]
    [Google Scholar]
  45. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article][PubMed]
    [Google Scholar]
  46. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17:540–552 [View Article][PubMed]
    [Google Scholar]
  47. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article][PubMed]
    [Google Scholar]
  48. 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]
  49. Whelan S, Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 2001; 18:691–699 [View Article][PubMed]
    [Google Scholar]
  50. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  51. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM et al. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 2014; 42:D633–D642 [View Article][PubMed]
    [Google Scholar]
  52. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  53. Nei M, Kumar S. Molecular Evolution and Phylogenetics Oxford University Press; 2000
    [Google Scholar]
  54. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  55. Chapaval L, Moon DH, Gomes JE, Duarte FR, Tsai SM. An alternative method for Staphylococcus aureus DNA isolation. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 2008; 60:299–306 [View Article]
    [Google Scholar]
  56. Chin CS, Alexander DH, Marks P, Klammer AA, Drake J et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 2013; 10:563–569 [View Article][PubMed]
    [Google Scholar]
  57. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article][PubMed]
    [Google Scholar]
  58. 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]
  59. 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]
  60. 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]
  61. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  62. Thompson CC, Chimetto L, Edwards RA, Swings J, Stackebrandt E et al. Microbial genomic taxonomy. BMC Genomics 2013; 14:913 [View Article][PubMed]
    [Google Scholar]
  63. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article][PubMed]
    [Google Scholar]
  64. Li J, Tai C, Deng Z, Zhong W, He Y et al. VRprofile: gene-cluster-detection-based profiling of virulence and antibiotic resistance traits encoded within genome sequences of pathogenic bacteria. Brief Bioinform 2018; 19:566–574 [View Article][PubMed]
    [Google Scholar]
  65. Core Team R. R: A Language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2016 http://www.R-project.org/
  66. Wickham H, Francois R, Henry L, Müller K. dplyr: A grammar of data manipulation. R package version (0.7.6.); 2018. https://CRAN.R-project.org/package=dplyr
  67. Carson DA, Barkema HW, Naushad S, De Buck J. Bacteriocins of non-aureus Staphylococci isolated from bovine milk. Appl Environ Microbiol 2017; 83:e0101501017 [View Article][PubMed]
    [Google Scholar]
  68. Clinical and Laboratory Standards Institute (CLSI) Performance Standards for Antimicrobial Susceptibility Testing Pennsylvania USA: Wayne; 2016
    [Google Scholar]
  69. Chopra I, Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 2001; 65:232–260 [View Article][PubMed]
    [Google Scholar]
  70. Naushad HS, Lee B, Gupta RS. Conserved signature indels and signature proteins as novel tools for understanding microbial phylogeny and systematics: identification of molecular signatures that are specific for the phytopathogenic genera Dickeya, Pectobacterium and Brenneria . Int J Syst Evol Microbiol 2014; 64:366–383 [View Article][PubMed]
    [Google Scholar]
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