1887

Abstract

The large-scale and high-intensity application of species in milk fermentation processes is associated with a persistent threat of (bacterio)phage infection. Phage infection of starter cultures may cause inconsistent, slow or even failed fermentations with consequent diminished product quality and/or output. The phage life cycle commences with the recognition of, and binding to, a specific host-encoded and surface-exposed receptor, which in the case of can be the rhamnose-glucose polysaccharide (RGP; specified by the gene cluster) or exopolysaccharide (EPS; specified by the gene cluster). The genomic diversity of 23 . strains isolated from unpasteurized dairy products was evaluated, including a detailed analysis of the and loci. In the present study, five novel genotypes were identified while variations of currently recognized gene cluster types were also observed. Furthermore, the diversity of genotypes amongst retrieved isolates positively correlated with phage diversity based on phageome analysis of eight representative dairy products. Our findings therefore substantially expand our knowledge on strain and phage diversity in (artisanal) dairy products and highlight the merit of phageome analysis of artisanal and traditional fermented foods as a sensitive marker of dominant microbiota involved in the fermentation.

Funding
This study was supported by the:
  • Science Foundation Ireland (Award 13/IA/1953)
    • Principle Award Recipient: Douwevan Sinderen
  • Science Foundation Ireland (Award 15/SIRG/3430)
    • Principle Award Recipient: JenniferMahony
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-04-20
2024-12-13
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References

  1. Parlindungan E, McDonnell B, Lugli GA, Ventura M, van Sinderen D et al. Dairy streptococcal cell wall and exopolysaccharide genome diversity. Figshare 2022 [View Article]
    [Google Scholar]
  2. Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D et al. New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol Rev 2005; 29:435–463 [View Article] [PubMed]
    [Google Scholar]
  3. Yamamoto E, Watanabe R, Koizumi A, Ishida T, Kimura K. Isolation and characterization of Streptococcus thermophilus possessing prts gene from raw milk in Japan. Biosci Microbiota Food Health 2020; 39:169–174
    [Google Scholar]
  4. Song A-L, In LLA, Lim SHE, Rahim RA. A review on Lactococcus lactis: from food to factory. Microb Cell Fact 2017; 16:55 [View Article] [PubMed]
    [Google Scholar]
  5. 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]
  6. EFSA Panel on Biological Hazards (BIOHAZ) Koutsoumanis K, Allende A, Álvarez-Ordóñez A, Bolton D et al. Update of the list of QPS-recommended biological agents intentionally added to food or feed as notified to EFSA 9: suitability of taxonomic units notified to EFSA until September 2018. EFSA J 2019; 17:e05555 [View Article] [PubMed]
    [Google Scholar]
  7. Mahony J, van Sinderen D. Novel strategies to prevent or exploit phages in fermentations, insights from phage-host interactions. Curr Opin Biotechnol 2015; 32:8–13 [View Article] [PubMed]
    [Google Scholar]
  8. Le Marrec C, van Sinderen D, Walsh L, Stanley E, Vlegels E et al. Two groups of bacteriophages infecting Streptococcus thermophilus can be distinguished on the basis of mode of packaging and genetic determinants for major structural proteins. Appl Environ Microbiol 1997; 63:3246–3253 [View Article] [PubMed]
    [Google Scholar]
  9. Mills S, Griffin C, O’Sullivan O, Coffey A, McAuliffe OE et al. A new phage on the ‘Mozzarella’ block: Bacteriophage 5093 shares A low level of homology with other Streptococcus thermophilus phages. Int Dairy J 2011; 21:963–969 [View Article]
    [Google Scholar]
  10. McDonnell B, Mahony J, Neve H, Hanemaaijer L, Noben J-P et al. Identification and analysis of a novel group of bacteriophages infecting the lactic acid bacterium Streptococcus thermophilus. Appl Environ Microbiol 2016; 82:5153–5165 [View Article] [PubMed]
    [Google Scholar]
  11. Philippe C, Levesque S, Dion MB, Tremblay DM, Horvath P et al. Novel genus of phages infecting Streptococcus thermophilus: genomic and morphological characterization. Appl Environ Microbiol 2020; 86:e00227-20 [View Article] [PubMed]
    [Google Scholar]
  12. Lavelle K, Martinez I, Neve H, Lugli GA, Franz CMAP et al. Biodiversity of Streptococcus thermophilus phages in global dairy fermentations. Viruses 2018; 10:E577 [View Article] [PubMed]
    [Google Scholar]
  13. Szymczak P, Janzen T, Neves AR, Kot W, Hansen LH et al. Novel variants of Streptococcus thermophilus bacteriophages are indicative of genetic recombination among phages from different bacterial species. Appl Environ Microbiol 2017; 83:e02748-16 [View Article] [PubMed]
    [Google Scholar]
  14. Quiberoni A, Tremblay D, Ackermann HW, Moineau S, Reinheimer JA. Diversity of Streptococcus thermophilus phages in a large-production cheese factory in Argentina. J Dairy Sci 2006; 89:3791–3799 [View Article] [PubMed]
    [Google Scholar]
  15. Dugat-Bony E, Lossouarn J, De Paepe M, Sarthou A-S, Fedala Y et al. Viral metagenomic analysis of the cheese surface: A comparative study of rapid procedures for extracting viral particles. Food Microbiol 2020; 85:103278 [View Article] [PubMed]
    [Google Scholar]
  16. Muhammed MK, Kot W, Neve H, Mahony J, Castro-Mejía JL et al. Metagenomic analysis of dairy bacteriophages: extraction method and pilot study on whey samples derived from using undefined and defined mesophilic starter cultures. Appl Environ Microbiol 2017; 83:e00888-17 [View Article] [PubMed]
    [Google Scholar]
  17. Romero DA, Magill D, Millen A, Horvath P, Fremaux C. Dairy lactococcal and streptococcal phage-host interactions: an industrial perspective in an evolving phage landscape. FEMS Microbiol Rev 2020; 44:909–932 [View Article] [PubMed]
    [Google Scholar]
  18. McDonnell B, Hanemaaijer L, Bottacini F, Kelleher P, Lavelle K et al. A cell wall-associated polysaccharide is required for bacteriophage adsorption to the Streptococcus thermophilus cell surface. Mol Microbiol 2020; 114:31–45 [View Article] [PubMed]
    [Google Scholar]
  19. Szymczak P, Filipe SR, Covas G, Vogensen FK, Neves AR et al. Cell wall glycans mediate recognition of the dairy bacterium Streptococcus thermophilus by bacteriophages. Appl Environ Microbiol 2018; 84:e01847-18 [View Article] [PubMed]
    [Google Scholar]
  20. Szymczak P, Rau MH, Monteiro JM, Pinho MG, Filipe SR et al. A comparative genomics approach for identifying host-range determinants in Streptococcus thermophilus bacteriophages. Sci Rep 2019; 9:7991 [View Article] [PubMed]
    [Google Scholar]
  21. Wu Q, Tun HM, Leung F-C, Shah NP. Genomic insights into high exopolysaccharide-producing dairy starter bacterium Streptococcus thermophilus ASCC 1275. Sci Rep 2014; 4:4974 [View Article] [PubMed]
    [Google Scholar]
  22. Kouwen RHM, Van Sinderen D, McDonnell B, Ver Loren Van Themaat P. Emiel Mahony J, inventors Streptococcus thermophilus starter cultures. Netherlands Patent 2019; 20190367866:
    [Google Scholar]
  23. Delorme C, Legravet N, Jamet E, Hoarau C, Alexandre B et al. Study of Streptococcus thermophilus population on a world-wide and historical collection by a new MLST scheme. Int J Food Microbiol 2017; 242:70–81 [View Article] [PubMed]
    [Google Scholar]
  24. Stern A, Sorek R. The phage-host arms race: shaping the evolution of microbes. Bioessays 2011; 33:43–51 [View Article] [PubMed]
    [Google Scholar]
  25. Burrus V, Bontemps C, Decaris B, Guédon G. Characterization of a novel type II restriction-modification system, Sth368I, encoded by the integrative element ICESt1 of Streptococcus thermophilus CNRZ368. Appl Environ Microbiol 2001; 67:1522–1528 [View Article] [PubMed]
    [Google Scholar]
  26. Common J, Morley D, Westra ER, van Houte S. CRISPR-Cas immunity leads to a coevolutionary arms race between Streptococcus thermophilus and lytic phage. Philos Trans R Soc Lond B Biol Sci 2019; 374:1772 [View Article] [PubMed]
    [Google Scholar]
  27. Achigar R, Scarrone M, Rousseau GM, Philippe C, Machado F et al. Ectopic spacer acquisition in Streptococcus thermophilus CRISPR3 Array. Microorganisms 2021; 9:512 [View Article] [PubMed]
    [Google Scholar]
  28. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P et al. The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res 2011; 39:9275–9282 [View Article] [PubMed]
    [Google Scholar]
  29. Horvath P, Romero DA, Coûté-Monvoisin A-C, Richards M, Deveau H et al. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 2008; 190:1401–1412 [View Article] [PubMed]
    [Google Scholar]
  30. Achigar R, Magadán AH, Tremblay DM, Julia Pianzzola M, Moineau S. Phage-host interactions in Streptococcus thermophilus: Genome analysis of phages isolated in Uruguay and ectopic spacer acquisition in CRISPR array. Sci Rep 2017; 7:43438 [View Article] [PubMed]
    [Google Scholar]
  31. Hu T, Cui Y, Qu X. Characterization and comparison of CRISPR Loci in Streptococcus thermophilus. Arch Microbiol 2020; 202:695–710 [View Article] [PubMed]
    [Google Scholar]
  32. Dion MB, Labrie SJ, Shah SA, Moineau S. CRISPRStudio: A User-Friendly Software for Rapid CRISPR Array Visualization. Viruses 2018; 10:E602 [View Article] [PubMed]
    [Google Scholar]
  33. Moh LG, Etienne PT, Jules-Roger K. Seasonal diversity of lactic acid bacteria in artisanal yoghurt and their antibiotic susceptibility pattern. Int J Food Sci 2021; 2021:6674644 [View Article] [PubMed]
    [Google Scholar]
  34. Fagbemigun O, Cho G-S, Rösch N, Brinks E, Schrader K et al. Isolation and characterization of potential starter cultures from the nigerian fermented milk product nono. Microorganisms 2021; 9:640 [View Article] [PubMed]
    [Google Scholar]
  35. Peng C, Sun Z, Sun Y, Ma T, Li W et al. Characterization and association of bacterial communities and nonvolatile components in spontaneously fermented cow milk at different geographical distances. J Dairy Sci 2021; 104:2594–2605 [View Article] [PubMed]
    [Google Scholar]
  36. Zago M, Bardelli T, Rossetti L, Nazzicari N, Carminati D et al. Evaluation of bacterial communities of Grana Padano cheese by DNA metabarcoding and DNA fingerprinting analysis. Food Microbiol 2021; 93:103613 [View Article] [PubMed]
    [Google Scholar]
  37. Hu T, Cui Y, Zhang Y, Qu X, Zhao C. Genome analysis and physiological characterization of four Streptococcus thermophilus strains isolated from Chinese traditional fermented milk. Front Microbiol 2020; 11:184 [View Article] [PubMed]
    [Google Scholar]
  38. Alexandraki V, Kazou M, Blom J, Pot B, Papadimitriou K et al. Comparative genomics of Streptococcus thermophilus support important traits concerning the evolution, biology and technological properties of the species. Front Microbiol 2019; 10:2916 [View Article] [PubMed]
    [Google Scholar]
  39. Lugli GA, Milani C, Mancabelli L, van Sinderen D, Ventura M. MEGAnnotator: A user-friendly pipeline for microbial genomes assembly and annotation. FEMS Microbiol Lett 2016; 363:fnw049 [View Article] [PubMed]
    [Google Scholar]
  40. 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]
  41. Chevreux B, Wetter T, Suhai S. eds Genome Sequence Assembly Using Trace Signals and Additional Sequence Information German Conference on Bioinformatics; 1999
    [Google Scholar]
  42. Rodriguez-R LM, Gunturu S, Harvey WT, Rosselló-Mora R, Tiedje JM et al. The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level. Nucleic Acids Res 2018; 46:W282–W288 [View Article] [PubMed]
    [Google Scholar]
  43. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–21 [View Article] [PubMed]
    [Google Scholar]
  44. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: A fast phage search tool. Nucleic Acids Res 2011; 39:W347–52 [View Article] [PubMed]
    [Google Scholar]
  45. Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA et al. Pfam: The protein families database in 2021. Nucleic Acids Res 2021; 49:D412–D419 [View Article] [PubMed]
    [Google Scholar]
  46. Enright AJ, Van Dongen S, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002; 30:1575–1584 [View Article] [PubMed]
    [Google Scholar]
  47. Saeed AI, Sharov V, White J, Li J, Liang W et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003; 34:374–378 [View Article] [PubMed]
    [Google Scholar]
  48. Milani C, Casey E, Lugli GA, Moore R, Kaczorowska J et al. Tracing mother-infant transmission of bacteriophages by means of a novel analytical tool for shotgun metagenomic datasets: METAnnotatorX. Microbiome 2018; 6:145 [View Article] [PubMed]
    [Google Scholar]
  49. Patel RK, Jain M. NGS QC Toolkit: A toolkit for quality control of next generation sequencing data. PLOS ONE 2012; 7:e30619 [View Article] [PubMed]
    [Google Scholar]
  50. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
    [Google Scholar]
  51. Lillehaug D. An improved plaque assay for poor plaque-producing temperate lactococcal bacteriophages. J Appl Microbiol 1997; 83:85–90 [View Article] [PubMed]
    [Google Scholar]
  52. Chuard C, Reller LB. Bile-esculin test for presumptive identification of enterococci and streptococci: effects of bile concentration, inoculation technique, and incubation time. J Clin Microbiol 1998; 36:1135–1136 [View Article] [PubMed]
    [Google Scholar]
  53. Delorme C, Bartholini C, Bolotine A, Ehrlich SD, Renault P. Emergence of a cell wall protease in the Streptococcus thermophilus population. Appl Environ Microbiol 2010; 76:451–460 [View Article] [PubMed]
    [Google Scholar]
  54. Kelleher P, Mahony J, Schweinlin K, Neve H, Franz CM et al. Assessing the functionality and genetic diversity of lactococcal prophages. Int J Food Microbiol 2018; 272:29–40 [View Article] [PubMed]
    [Google Scholar]
  55. Arioli S, Eraclio G, Della Scala G, Neri E, Colombo S et al. Role of temperate bacteriophage ϕ20617 on Streptococcus thermophilus DSM 20617T autolysis and biology. Front Microbiol 2018; 9:2719 [View Article]
    [Google Scholar]
  56. Mahony J, Bottacini F, van Sinderen D, Fitzgerald GF. Progress in lactic acid bacterial phage research. Microb Cell Fact 2014; 13 Suppl 1:S1 [View Article] [PubMed]
    [Google Scholar]
  57. Paez-Espino D, Sharon I, Morovic W, Stahl B, Thomas BC et al. CRISPR immunity drives rapid phage genome evolution in Streptococcus thermophilus. mBio 2015; 6:e00262-15 [View Article] [PubMed]
    [Google Scholar]
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