Skip to content
1887

Abstract

is widely used as a starter culture in the production of cheese, yoghurt and various cultured dairy products, which holds considerable significance in both research and practical applications within the food industry. Throughout history, the taxonomy of has undergone several adjustments and revisions. In 1984, based on the result of DNA–DNA hybridization, was reclassified as subsp. . Subsequently, in 1991, Schleifer . proposed the revival of the species also relying on a DNA–DNA hybridization study conducted under stringent conditions. At present, both the taxonomic names, and subsp. , are considered as synonyms and adopted within scientific research, regulatory oversight and relevant industries, leading to a certain degree of confusion. A precise and scientifically accurate taxonomic status is imperative as a foundational prerequisite for a strain evaluation and its application in food manufacture and regulatory contexts. In this study, we utilized whole-genome sequencing to evaluate the genetic relationship of and . At the gene level, phylogenetic analyses were conducted on 52 . strains and 63 . strains based on sequences of both the 16S rRNA gene and the housekeeping gene, . Additionally, a core-gene phylogeny was inferred using the whole-genome sequencing data of 216 strains within the genus. This analysis facilitated an exhaustive evaluation of the evolutionary interconnections among the studied strains. At the genetic level, average nucleotide identity (ANI) and digital DNA–DNA hybridization (dDDH) were used to verify the species identity of and . The results of phylogenetic analysis, ANI and dDDH all collectively confirm that and are distinct species. These research results provide sufficient scientific evidence to support the definitive scientific and rational application of the name of .

Funding
This study was supported by the:
  • National Infrastructure for Microbiological Resources (Award Fund of National Microbial Resource Center (number NMRC 2024-4))
    • Principal Award Recipient: NotApplicable
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006612
2025-01-21
2026-01-20

Metrics

Loading full text...

Full text loading...

References

  1. Orla-Jensen S. The Lactic Acid Bacteria Copenhagen: Host and Son; pp 1–196
    [Google Scholar]
  2. Harnett J, Davey G, Patrick A, Caddick C, Pearce L. Lactic acid bacteria | Streptococcus thermophilus. Encycl Dairy Sci 2011143–148 [View Article]
    [Google Scholar]
  3. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD et al. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat Biotechnol 2004; 22:1554–1558 [View Article] [PubMed]
    [Google Scholar]
  4. Andrewes FW, Horder TJ. A study of the streptococci pathogenic for man. Lancet 1906; 168:708–713 [View Article]
    [Google Scholar]
  5. Roger P, Delettre J, Bouix M, Béal C. Characterization of Streptococcus salivarius growth and maintenance in artificial saliva. J Appl Microbiol 2011; 111:631–641 [View Article] [PubMed]
    [Google Scholar]
  6. Delorme C, Abraham A-L, Renault P, Guédon E. Genomics of Streptococcus salivarius, a major human commensal. Infect Genet Evol 2015; 33:381–392 [View Article] [PubMed]
    [Google Scholar]
  7. Ottogalli G, Galli A, Dellaglio F. Taxonomic relationships between Streptococcus thermophilus and some other streptococci. J Dairy Res 1979; 46:127–131 [View Article]
    [Google Scholar]
  8. Kilpper-Bälz R, Fischer G, Schleifer KH. Nucleic acid hybridization of group N and group D streptococci. Curr Microbiol 1982; 7:245–250 [View Article]
    [Google Scholar]
  9. Sneath PHA, McGOWAN V, Skerman VBD. Approved lists of bacterial names. Int J Syst Bacteriol 1980; 30:225–420 [View Article]
    [Google Scholar]
  10. Farrow JAE, Collins MD. DNA base composition, DNA-DNA homology and long-chain fatty acid studies on Streptococcus thermophilus and Streptococcus salivarius. J Gen Microbiol 1984; 130:357–362 [View Article] [PubMed]
    [Google Scholar]
  11. Schleifer KH, Ehrmann M, Krusch U, Neve H. Revival of the species Streptococcus thermophilus (ex Orla-Jensen, 1919) nom. rev. Syst Appl Microbiol 1991; 14:386–388 [View Article]
    [Google Scholar]
  12. Federation ID. IDF position paper on clarifying taxonomy of dairy starter culture Streptococcus thermophilus; 2024 https://shop.fil-idf.org/products/idf-position-paper-on-clarifying-taxonomy-of-dairy-starter-culture-streptococcus-thermophilus
  13. Cho H, Park KE, Kim KS. Genome analysis of Streptococcus salivarius subsp. thermophilus type strain ATCC 19258 and its comparison to equivalent strain NCTC 12958. Arch Microbiol 2021; 203:1843–1849 [View Article] [PubMed]
    [Google Scholar]
  14. Shani N, Isolini D, Marzohl D, Berthoud H. Evaluation of a new culture medium for the enumeration and isolation of Streptococcus salivarius subsp. thermophilus from cheese. Food Microbiol 2021; 95:103672 [View Article] [PubMed]
    [Google Scholar]
  15. Roux E, Nicolas A, Valence F, Siekaniec G, Chuat V et al. The genomic basis of the Streptococcus thermophilus health-promoting properties. BMC Genom 2022; 23:210 [View Article] [PubMed]
    [Google Scholar]
  16. Han M, Wu Y, Guo X, Jiang L, Wang X et al. Milk fermentation by monocultures or co-cultures of Streptococcus thermophilus strains. Front Bioeng Biotechnol 2022; 10:1097013 [View Article] [PubMed]
    [Google Scholar]
  17. Johnson JL, Ordal EJ. Deoxyribonucleic acid homology in bacterial taxonomy: effect of incubation temperature on reaction specificity. J Bacteriol 1968; 95:893–900 [View Article] [PubMed]
    [Google Scholar]
  18. Schleifer KH, Stackebrandt E. Molecular systematics of prokaryotes. Annu Rev Microbiol 1983; 37:143–187 [View Article] [PubMed]
    [Google Scholar]
  19. Schildkraut CL, Marmur J, Doty P. The formation of hybrid DNA molecules and their use in studies of DNA homologies. J Mol Biol 1961; 3:595–617 [View Article] [PubMed]
    [Google Scholar]
  20. McCarthy BJ, Bolton ET. An approach to the measurement of genetic relatedness among organisms. Proc Natl Acad Sci U S A 1963; 50:156–164 [View Article] [PubMed]
    [Google Scholar]
  21. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  22. 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]
  23. 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]
  24. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article] [PubMed]
    [Google Scholar]
  25. Arahal DR. Whole-genome analyses: average nucleotide identity. In Goodfellow M, Sutcliffe I, Chun J. eds Methods in Microbiology Academic Press; 2014 pp 103–122 [View Article]
    [Google Scholar]
  26. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  27. 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]
  28. Lagesen K, Hallin P, Rødland EA, Staerfeldt H-H, Rognes T et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108 [View Article] [PubMed]
    [Google Scholar]
  29. 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]
  30. 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]
  31. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
    [Google Scholar]
  32. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article] [PubMed]
    [Google Scholar]
  33. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinform 2009; 10:421 [View Article] [PubMed]
    [Google Scholar]
  34. Delcher AL, Bratke KA, Powers EC, Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 2007; 23:673–679 [View Article] [PubMed]
    [Google Scholar]
  35. 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]
  36. Hayashi Sant’Anna F, Bach E, Porto RZ, Guella F, Hayashi Sant’Anna E et al. Genomic metrics made easy: what to do and where to go in the new era of bacterial taxonomy. Crit Rev Microbiol 2019; 45:182–200 [View Article] [PubMed]
    [Google Scholar]
  37. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 2016; 8:12–24 [View Article]
    [Google Scholar]
  38. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article] [PubMed]
    [Google Scholar]
  39. Chen C, Chen H, Zhang Y, Thomas HR, Frank MH et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 2020; 13:1194–1202 [View Article]
    [Google Scholar]
  40. Bosshard PP, Zbinden R, Abels S, Böddinghaus B, Altwegg M et al. 16S rRNA gene sequencing versus the API 20 NE system and the VITEK 2 ID-GNB card for identification of nonfermenting Gram-negative bacteria in the clinical laboratory. J Clin Microbiol 2006; 44:1359–1366 [View Article] [PubMed]
    [Google Scholar]
  41. Pombert J-F, Sistek V, Boissinot M, Frenette M. Evolutionary relationships among salivarius streptococci as inferred from multilocus phylogenies based on 16S rRNA-encoding, recA, secA, and secY gene sequences. BMC Microbiol 2009; 9:232 [View Article] [PubMed]
    [Google Scholar]
  42. Mignard S, Flandrois JP. 16S rRNA sequencing in routine bacterial identification: a 30-month experiment. J Microbiol Methods 2006; 67:574–581 [View Article] [PubMed]
    [Google Scholar]
  43. Kawamura Y, Hou X-G, Sultana F, Miura H, Ezaki T. Determination of 16S rRNA sequences of Streptococcus mitis and Streptococcus gordonii and phylogenetic relationships among members of the genus Streptococcus. Int J Syst Evol Microbiol 1995; 45:406–408 [View Article]
    [Google Scholar]
  44. Hardie JM, Whiley RA. Classification and overview of the genera Streptococcus and Enterococcus. J Appl Microbiol 1997; 83:1S–11S [View Article] [PubMed]
    [Google Scholar]
  45. Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol Biol Evol 2017; 34:2115–2122 [View Article] [PubMed]
    [Google Scholar]
  46. Corredoira JC, Alonso MP, García JF, Casariego E, Coira A et al. Clinical characteristics and significance of Streptococcus salivarius bacteremia and Streptococcus bovis bacteremia: a prospective 16-year study. Eur J Clin Microbiol Infect Dis 2005; 24:250–255 [View Article] [PubMed]
    [Google Scholar]
  47. Iyer R, Tomar SK, Uma Maheswari T, Singh R. Streptococcus thermophilus strains: multifunctional lactic acid bacteria. Int Dairy J 2010; 20:133–141 [View Article]
    [Google Scholar]
  48. Koutsoumanis K, Allende A, Álvarez‐Ordóñez A, Bolton D, Bover‐Cid S et al. Update of the list of qualified presumption of safety (QPS) recommended microorganisms intentionally added to food or feed as notified to EFSA. EFS2 2023; 21:e07747 [View Article]
    [Google Scholar]
  49. Rosselló-Mora R, Amann R. The species concept for prokaryotes. FEMS Microbiol Rev 2001; 25:39–67 [View Article] [PubMed]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.006612
Loading
/content/journal/ijsem/10.1099/ijsem.0.006612
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An error occurred
Approval was partially successful, following selected items could not be processed due to error