Skip to main content
SpringerLink
Log in

Genetic diversity and phylogenetic relationships of Streptococcus thermophilus isolates from traditional Turkish yogurt: multilocus sequence typing (MLST)

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Yogurt, a globally consumed fermented dairy product, is recognized for its taste and potential health benefits attributed to probiotic bacteria, particularly Streptococcus thermophilus. In this study, we employed Multilocus Sequence Typing (MLST) to investigate the genetic diversity and phylogenetic relationships of 13 S. thermophilus isolates from traditional Turkish yogurt samples. We also assessed potential correlations between genetic traits and geographic origins. The isolates were identified as S. thermophilus using VITEK® MALDI-TOF MS, ribotyping, and 16S rRNA analysis methods. MLST analysis revealed 13 different sequence types (STs), with seven new STs for Turkey. The most prevalent STs were ST/83 (n = 3), ST/135 (n = 2), and ST/134 (n = 2). eBURST analysis showed that these isolates mainly were singletons (n = 7) defined as sequence types (STs) that cannot be assigned to any group and differ at two or more alleles from every other ST in the sample. This information suggests that the isolates under study were genetically distinct from the other isolates in the dataset, highlighting their unique genetic profiles within the population. Genetic diversity analysis of ten housekeeping genes revealed polymorphism, with some genes showing higher allelic variation than others. Tajima’s D values suggested that selection pressures differed among these genes, with some being more conserved, likely due to their vital functions. Phylogenetic analysis revealed distinct genetic diversity between Turkish isolates and European and Asian counterparts. These findings demonstrate the genetic diversity of S. thermophilus isolates in Turkish yogurt and highlight their unique evolutionary patterns. This research contributes to our understanding of local microbial diversity associated with yogurt production in Turkey and holds the potential for identifyic strains with enhanced functional attributes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Availability of data and materials

Data and materials used in this study are available upon request. In addition, the data of the isolates used in this study can be found in NCBI BioProject Number PRJNA914520.

References

  • Alexandraki V, Kazou M, Blom J, Pot B, Papadimitriou K, Tsakalidou E (2019) Comparative genomics of Streptococcus thermophilus support important traits concerning the evolution, biology and technological properties of the species. Front Microbiol 10:2916

    Article  PubMed  PubMed Central  Google Scholar 

  • Arnold BJ, Huang I-T, Hanage WP (2022) Horizontal gene transfer and adaptive evolution in bacteria. Nat Rev Microbiol 20(4):206–218

    Article  PubMed  CAS  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477

    Article  MathSciNet  PubMed  PubMed Central  CAS  Google Scholar 

  • Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, Kulakauskas S, Lapidus A, Goltsman E, Mazur M, Pusch GD (2004) Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat Biotechnol 22(12):1554–1558

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dan T, Liu W, Sun Z, Lv Q, Xu H, Song Y, Zhang H (2014) A novel multi-locus sequence typing (MLST) protocol for Leuconostoc lactis isolates from traditional dairy products in China and Mongolia. BMC Microbiol 14(1):1–9

    Article  Google Scholar 

  • Delorme C, Bartholini C, Bolotine A, Ehrlich SD, Renault P (2010) Emergence of a cell wall protease in the Streptococcus thermophilus population. Appl Environ Microbiol 76(2):451–460

    Article  PubMed  ADS  CAS  Google Scholar 

  • Delorme C, Legravet N, Jamet E, Hoarau C, Alexandre B, El-Sharoud WM, Darwish MS, Renault P (2017) Study of Streptococcus thermophilus population on a world-wide and historical collection by a new MLST scheme. Int J Food Microbiol 242:70–81

    Article  PubMed  Google Scholar 

  • Demirci T, Akın N, Öztürk Hİ, Oğul A (2022) A metagenomic approach to homemade back-slopped yogurts produced in mountainous villages of Turkey with the potential next-generation probiotics. LWT 154:112860

    Article  CAS  Google Scholar 

  • Dikmen H, Goktas H, Demirbas F, Kayacan S, Ispirli H, Arici M, Turker M, Sagdic O, Dertli E (2023) Multilocus sequence typing of L. bulgaricus and S. thermophilus strains from Turkish traditional yoghurts and characterisation of their techno-functional roles. Food Sci Biotechnol 1–11

  • Fernandez MA, Marette A (2017) Potential health benefits of combining yogurt and fruits based on their probiotic and prebiotic properties. Adv Nutr 8(1):155S-164S

    Article  PubMed  PubMed Central  Google Scholar 

  • Francisco AP, Bugalho M, Ramirez M, Carriço JA (2009) Global optimal eBURST analysis of multilocus typing data using a graphic matroid approach. BMC Bioinf 10:1–15

    Article  Google Scholar 

  • Hafeez Z, Cakir-Kiefer C, Girardet J-M, Jardin J, Perrin C, Dary A, Miclo L (2013) Hydrolysis of milk-derived bioactive peptides by cell-associated extracellular peptidases of Streptococcus thermophilus. Appl Microbiol Biotechnol 97:9787–9799

    Article  PubMed  CAS  Google Scholar 

  • Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N, Decaris B, Bolotin A, Delorme C, Dusko Ehrlich S (2005) New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol Rev 29(3):435–463

    PubMed  CAS  Google Scholar 

  • Hu T, Cui Y, Zhang Y, Qu X, Zhao C (2020) Genome analysis and physiological characterization of four Streptococcus thermophilus strains isolated from Chinese traditional fermented milk. Front Microbiol 11:184

    Article  PubMed  PubMed Central  Google Scholar 

  • Jolley KA, Bray JE, Maiden MC (2018) Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 3:124

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Tamura K, Nei M (1994) MEGA: molecular evolutionary genetics analysis software for microcomputers. Bioinformatics 10(2):189–191

    Article  CAS  Google Scholar 

  • Letunic I, Bork P (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39(suppl_2):W475–W478

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Linares DM, O’Callaghan TF, O’Connor PM, Ross RP, Stanton C (2016) Streptococcus thermophilus APC151 strain is suitable for the manufacture of naturally GABA-enriched bioactive yogurt. Front Microbiol 7:1876

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu W, Su X, Duo N, Yu J, Song Y, Sun T, Zha M, Menghe B, Zhang H, Sun Z (2019) A survey of the relationship between functional genes and acetaldehyde production characteristics in Streptococcus thermophilus by multilocus sequence typing. J Dairy Sci 102(11):9651–9662

    Article  PubMed  CAS  Google Scholar 

  • Madslien EH, Olsen JS, Granum PE, Blatny JM (2012) Genotyping of B. licheniformisbased on a novel multi-locus sequence typing (MLST) scheme. BMC Microbiol 12(1):1–8

    Article  Google Scholar 

  • Maiden MC, Van Rensburg MJJ, Bray JE, Earle SG, Ford SA, Jolley KA, McCarthy ND (2013) MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 11(10):728–736

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mora D, Fortina M, Parini C, Ricci G, Gatti M, Giraffa G, Manachini P (2002) Genetic diversity and technological properties of Streptococcus thermophilus strains isolated from dairy products. J Appl Microbiol 93(2):278–287

    Article  PubMed  CAS  Google Scholar 

  • Nagaoka S (2019) Yogurt production. Lactic acid bacteria: Methods and protocols, 45–54.

  • Nascimento M, Sousa A, Ramirez M, Francisco AP, Carriço JA, Vaz C (2017) PHYLOViZ 2.0: providing scalable data integration and visualization for multiple phylogenetic inference methods. Bioinformatics 33(1):128–129

    Article  PubMed  CAS  Google Scholar 

  • National Dairy Council (2019) Dünya ve Türkiye’de Süt Sektörü İstatistikleri 2019. Ulusal Süt Konseyi Yayınları 1. Basım, Ankara http://www.ulusalsutkonseyi.org.tr/wp-content/uploads/Ulusal-Sut-Konseyi-Sut-Raporu-2019.pdf. Accessed January 2024

  • Pichler M, Coskun ÖK, Ortega-Arbulú AS, Conci N, Wörheide G, Vargas S, Orsi WD (2018) A 16S rRNA gene sequencing and analysis protocol for the Illumina MiniSeq platform. Microbiologyopen 7(6):e00611

    Article  PubMed  PubMed Central  Google Scholar 

  • Roux E, Nicolas A, Valence F, Siekaniec G, Chuat V, Nicolas J, Le Loir Y, Guédon E (2022) The genomic basis of the Streptococcus thermophilus health-promoting properties. BMC Genomics 23(1):210

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Somerville V, Berthoud H, Schmidt RS, Bachmann H-P, Meng YH, Fuchsmann P, von Ah U, Engel P (2022) Functional strain redundancy and persistent phage infection in Swiss hard cheese starter cultures. ISME J 16(2):388–399

    Article  PubMed  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595

    Article  MathSciNet  PubMed  PubMed Central  CAS  Google Scholar 

  • Usui Y, Kimura Y, Satoh T, Takemura N, Ouchi Y, Ohmiya H, Kobayashi K, Suzuki H, Koyama S, Hagiwara S (2018) Effects of long-term intake of a yogurt fermented with Lactobacillus delbrueckii subsp. bulgaricus 2038 and Streptococcus thermophilus 1131 on mice. Int Immunol 30(7):319–331

    Article  PubMed  CAS  Google Scholar 

  • Vendramin V, Treu L, Campanaro S, Lombardi A, Corich V, Giacomini A (2017) Genome comparison and physiological characterization of eight Streptococcus thermophilus strains isolated from Italian dairy products. Food Microbiol 63:47–57

    Article  PubMed  CAS  Google Scholar 

  • Weller C, Wu M (2015) A generation-time effect on the rate of molecular evolution in bacteria. Evolution 69(3):643–652

    Article  PubMed  ADS  CAS  Google Scholar 

  • Xu H, Liu W, Zhang W, Yu J, Song Y, Menhe B, Zhang H, Sun Z (2015) Use of multilocus sequence typing to infer genetic diversity and population structure of Lactobacillus plantarum isolates from different sources. BMC Microbiol 15(1):1–10

    Article  Google Scholar 

  • Yu J, Sun Z, Liu W, Xi X, Song Y, Xu H, Lv Q, Bao Q, Menghe B, Sun T (2015) Multilocus sequence typing of Streptococcus thermophilus from naturally fermented dairy foods in China and Mongolia. BMC Microbiol 15(1):1–13

    Article  Google Scholar 

Download references

Funding

This study was carried out using the data obtained from the academic career project numbered TAGEM/HSGYAD/A/21/A3/P1/2311 by the General Directorate of Agricultural Research and Policy under the Ministry of Agriculture and Forestry.

Author information

Authors and Affiliations

  1. Animal Originated Foodstuffs Department, Central Research Institute of Food and Feed Control, Bursa, Turkey

    Deniz Kiraz & Ali Özcan

  2. Food Hygiene and Technology Department, Faculty of Veterinary Medicine, Uludağ University, Bursa, Turkey

    Ali Özcan & Artun Yibar

  3. Faculty of Chemistry and Metallurgy, Department of Food Engineering, Yildiz Technical University, Istanbul, Turkey

    Enes Dertli

Authors
  1. Deniz Kiraz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ali Özcan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Artun Yibar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Enes Dertli
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

DK research design, data collection and analysis, and writing and editing of the manuscript. AÖ literature review, data analysis, interpretation of results, and revision of the manuscript. AY statistical analysis, design of methods, and proofreading of the manuscript. ED supervision, guiding the research process, and final revision.

Corresponding author

Correspondence to Deniz Kiraz.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethics approval

There is no ethical concern in this study.

Additional information

Communicated by Yusuf Akhter.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 30 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kiraz, D., Özcan, A., Yibar, A. et al. Genetic diversity and phylogenetic relationships of Streptococcus thermophilus isolates from traditional Turkish yogurt: multilocus sequence typing (MLST). Arch Microbiol 206, 121 (2024). https://doi.org/10.1007/s00203-024-03850-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00203-024-03850-7

Keywords

Search

Navigation