New insights into various production characteristics of streptococcus thermophilus strains

International Journal of Molecular Sciences

Volumn 17, Issue 10, 2016, Pages

  Cui, Yanhua ^a   Xu, Tingting ^a   Qu, Xiaojun ^b   Hu, Tong ^a   Jiang, Xu ^a   Zhao, Chunyu ^a  

^a HARBIN INSTITUTE OF TECHNOLOGY   (China)

^b Heilongjiang Academy of Sciences   (China)

Author keywords

Genomics; Plasmid; Production characteristics; Streptococcus thermophilus

Indexed keywords

FLAVORING AGENT; GALACTOSE;

AMINO ACID METABOLISM; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL METABOLISM; BACTERIAL STRAIN; BIOTECHNOLOGICAL PRODUCTION; CARBOHYDRATE METABOLISM; CARBOHYDRATE SYNTHESIS; FERMENTATION; GENETIC VARIABILITY; GLUCOSE UTILIZATION; MICROBIAL DIVERSITY; NONHUMAN; PHENOTYPE; PLASMID; PROTEIN DEGRADATION; REVIEW; STREPTOCOCCUS THERMOPHILUS; ANIMAL; CHEMISTRY; CLASSIFICATION; FOOD CONTROL; GENETICS; MICROBIOLOGY; MILK; PHYSIOLOGY; TRENDS;

ANIMALS; CARBOHYDRATE METABOLISM; FERMENTATION; FOOD MICROBIOLOGY; INDUSTRIAL MICROBIOLOGY; MILK; STREPTOCOCCUS THERMOPHILUS;

EID: 84991688480     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17101701     Document Type: Review

References (104)

1. Adolfsson, O.; Meydani, S.N.; Russell, R.M. Yogurt and gut function. Am. J. Clin. Nutr. 2004, 80, 245–256.
2. Iyer, R.; Tomar, S.K.; Maheswari, T.U.; Singh, R. Streptococcus thermophilus strains: Multifunctional lactic acid bacteria. Int. Dairy J. 2010, 20, 133–141.
3. Vaningelgem, F.; Zamfir, M.; Mozzi, F.; Adriany, T.; Vancanneyt, M. Biodiversity of exopolysaccharides produced by Streptococcus thermophilus strains is reflected in their production and their molecular and functional characteristics. Appl. Environ. Microbiol. 2004, 70, 900–912.
4. Hols, P.; Hancy, F.; Fontaine, L.; Grossiord, B.; Prozzi, D. New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol. Rev. 2005, 29, 435–463.
5. Zotta, T.; Ricciardi, A.; Ciocia, I F.; Rossano, R.; Parente, E. Diversity of stress responses in dairy thermophilic streptococci. Int. J. Food Microbiol. 2008, 124, 34–42.
6. Galia, W.; Perrin, C.; Genay, M. Variability and molecular typing of Streptococcus thermophilus strains displaying different proteolytic and acidifying properties. Int. Dairy J. 2009, 19, 89–95.
7. Vuyst, L.D.; Weckx, S.; Ravyts, F.; Herman, L.; Leroy, F. New insights into the exopolysaccharide production of Streptococcus thermophilus. Int. Dairy J. 2011, 21, 586–591.
8. Miclo, L.; Roux, É.; Genay, M.; Brusseaux, É.; Poirson, C.; Jameh, N.; Perrin, C.; Dary, A. Variability of hydrolysis of s1, and s2-Caseins by 10 strains of Streptococcus thermophilus and resulting bioactive peptides. J. Agric. Food Chem. 2012, 60, 554–565.
9. Rossi, F.; Marzotto, M.; Cremonese, S.; Rizzotti, L.; Torriani, S. Diversity of Streptococcus thermophilus in bacteriocin production, inhibitory spectrum and occurrence of thermophilin genes. Food Microbiol. 2013, 35, 27–33.
10. Bolotin, A.; Quinquis, B.; Renault, P.; Sorokin, A.; Ehrlich, S.D.; Kulakauskas, S.; Lapidus, A.; Goltsman, E.; Mazur, M.; Pusch, G.D., et al. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat. Biotechnol. 2004, 22, 1554–1558.
11. Delorme, C.; Bartholini, C.; Luraschi, M.; Pons, N.; Loux, V.; Almeida, M.; Guédon, E.; Gibrat, J.F.; Renault, P. Complete genome sequence of the pigmented Streptococcus thermophilus strain JIM8232. J. Bacteriol. 2011, 193, 5581–5582.
12. Makarova, K.; Slesarev, A.; Wolf, Y.; Sorokin, A.; Mirkin, B.; Koonin, E.; Pavlov, A.; Pavlova, N.; Karamychev, V.; Polouchine, N., et al. Comparative genomics of the lactic acid bacteria. Proc. Natl. Acad. Sci. USA 2006, 103, 15611–15616.
13. Sun, Z.; Chen, X.; Wang, J.; Zhao, W.; Shao, Y.; Wu, L.; Zhou, Z.; Sun, T.; Wang, L.; Meng, H., et al. Complete genome sequence of Streptococcus thermophilus strain ND03. J. Bacteriol. 2011, 193, 793–794.
14. Kang, X.; Ling, N.; Sun, G.; Zhou, Q.; Zhang, L.; Sheng, Q. Complete genome sequence of Streptococcus thermophilus strain MN-ZLW-002. J. Bacteriol. 2012, 194, 4428–4429.
15. Wu, Q.; Tun, H.M.; Leung, F.C.; Shah, N.P. Genomic insights into high exopolysaccharide-producing dairy starter bacterium Streptococcus thermophilus ASCC 1275. Sci. Rep. 2014, 4, 4974.
16. Labrie, S.J.; Tremblay, D.M.; Plante, P.L.; Wasserscheid, J.; Dewar, K.; Corbeil, J.; Moineau, S. Complete genome sequence of Streptococcus thermophilus SMQ-301, a model strain for phage-post interactions. Genome Announc. 2015, 3, e00480-15.
17. Shi, Y.; Chen, Y.; Li, Z.; Yang, L.; Chen, W.; Mu, Z. Complete genome sequence of Streptococcus thermophilus MN-BM-A02, a rare strain with a high acid-producing rate and low post-acidification ability. Genome Announc. 2015, 3, e00979-15.
18. Bai, Y.; Sun, E.; Shi, Y.D.; Jiang, Y.Y.; Chen, Y.; Liu, S.L.; Zhao, L.; Zhang, M.; Guo, H.Y.; Zhang, H., et al. Complete genome sequence of Streptococcus thermophilus MN-BM-A01, a strain with high exopolysaccharides production. J. Biotechnol. 2016, 224, 45–46.
19. Treu, L.; Vendramin, V.; Bovo, B.; Campanaro, S.; Corich, V.; Giacomini, A. Genome sequences of Streptococcus thermophilus strains MTH17CL396 and M17PTZA496 from Fontina, an Italian PDO cheese. Genome Announc. 2014, 2, e00067-14.
20. Treu, L.; Vendramin, V.; Bovo, B.; Campanaro, S.; Corich, V.; Giacominia, A. Whole-genome sequences of Streptococcus thermophilus strains TH1435 and TH1436, isolated from raw goat milk. Genome Announc. 2014, 2, e01129-13.
21. Treu, L.; Vendramin, V.; Bovo, B.; Campanaro, S.; Corich, V.; Giacomini, A. Genome sequences of four Italian Streptococcus thermophilus strains of dairy origin. Genome Announc. 2014, 2, e00126-14.
22. Prajapati, J.B.; Nathani, N.M.; Patel, A.K.; Senan, S.; Joshi, C.G. Genomic analysis of dairy starter culture Streptococcus thermophilus MTCC 5461. J. Microbiol. Biotechnol. 2013, 23, 459–466.
23. Barrangou, R.; Coute-Monvoisin, A.C.; Stahl, B.; Chavichvily, I.; Damange, F.; Romero, D.A.; Boyaval, P.; Fremaux, C.; Horvath, P. Genomic impact of CRISPR immunization against bacteriophages. Biochem. Soc. Trans. 2013, 41, 1383–1391.
24. Wels, M.; Serrano, L.M.; Eibrink, B.J.; Backus, L.; Bongers, R.S.; Vriesendorp, B.; Siezen, R.J.; van Hijum, S.A.; Meijer, W.C. Draft genome sequence of Streptococcus thermophilus C106, a dairy isolate from an artisanal cheese produced in the countryside of Ireland. Genome Announc. 2015, 3, e01377-15.
25. Goh, Y.J.; Goin, C.; O’Flaherty, S.; Altermann, E.; Hutkins, R. Specialized adaptation of a lactic acid bacterium to the milk environment: The comparative genomics of Streptococcus thermophilus LMD-9. Microb. Cell Factories 2011, 10 (Suppl. 1), 10066–10071.
26. Eng, C.; Thibessard, A.; Danielsen, M.; Rasmussen, T.B.; Mari, J.F.; Leblond, P. In silico prediction of horizontal gene transfer in Streptococcus thermophilus. Arch. Microbiol. 2011, 193, 287–297.
27. Liu, M.J.; Siezen, R.J.; Nauta, A. In silico prediction of horizontal gene transfer events in Latobacillus bulgaricus and Streptococcus thermophilus reveals protocooperation in yogurt manufacturing. Appl. Environ. Microbiol. 2009, 75, 4120–4129.
28. Rasmussen, T.B.; Danielsen, M.; Valina, O.; Garrigues, C.; Johansen, E.; Pedersen, M.B. Streptococcus thermophilus core genome: Comparative genome hybridization study of 47 strains. Appl. Environ. Microbiol. 2008, 74, 4703–4710.
29. Cui, Y.H.; Hu, T.; Qu, X.J.; Zhang, L.W.; Ding, Z.Q.; Dong, A.J. Plasmids from food lactic acid bacteria: Diversity, similarity, and new developments. Int. J. Mol. Sci. 2015, 16, 13172–13202.
30. Mercenier, A. Molecular genetics of Streptococcus thermophilus. FEMS Microbiol. Rev. 1990, 87, 61–78.
31. Somkuti, G.A.; Solaiman, D.K.Y.; Steinberg, D.H. Structural and functional properties of the hsp16.4-bearing plasmid pER341 in Streptococcus thermophilus. Plasmid 1998, 40, 61–72.
32. O’Sullivan, T.; van Sinderen, D.; Fitzgerald, G. Structural and functional analysis of pCI65st, a 6.5 kb plasmid from Streptococcus thermophilus NDI-6. Microbiology 1999, 145, 127–134.
33. Su, P.; Jury, K.; Allison, G.E.; Wong, W.Y.; Kim, W.S.; Liu, C.Q.; Vancov, T.; Dunn, N.W. Cloning vectors for Streptococcus thermophilus derived from a native plasmid. FEMS Microbiol. Lett. 2002, 216, 43–47.
34. Geis, A.E.; Demerdash, H.A.M.; Heller, K.J. Sequence analysis and characterization of plasmids from Streptococcus thermophilus. Plasmid 2003, 50, 53–69.
35. Petrova, P.; Miteva, V.; Ruiz-Maso, J.A.; Solar, G.D. Structural and functional analysis of pt38, a 2.9 kb plasmid of Streptococcus thermophilus yoghurt strain. Plasmid 2003, 50, 176–189.
36. Somkuti, G.A.; Steinberg, D.H. Promoter activity of the pER341-borne STphsp in heterologous gene expression in E. coli and Streptococcus thermophilus. FEMS Microbiol. Lett. 1999, 179, 431–436.
37. Solow, B.T.; Somkuti, G.A. Comparison of low-molecular-weight heat stress proteins encoded on plasmids in different strains of Streptococcus thermophilus. Curr. Microbiol. 2000, 41, 177–181.
38. Turgeon, N.; Moineau, S. Isolation and characterization of a Streptococcus thermophilus plasmid closely related to the pMV158 family. Plasmid 2001, 45, 171–183.
39. Girard, S.L.; Moineau, S. Analysis of two _-replicating plasmids of Streptococcus thermophilus. Plasmid 2007, 58, 174–181.
40. O’Leary, V.S.; Woychik, J.H. Utilization of lactose, glucose, and galactose by a mixed culture of Streptococcus thermophilus and Lactobacillus bulgaricus in milk treated with lactase enzyme. Appl. Environ. Microbiol. 1976, 32, 89–94.
41. Tinson, W.; Ratcliff, M.F.; Hillier, A.J.; Jago, G.R. Metabolism of Streptococcus thermophilus. 3. Influence on the level of bacterial metabolites in Cheddar cheese. Aust. J. Dairy Technol. 1982, 37, 17–21.
42. De Vin, F.; Rådström, P.; Herman, L.; de Vuyst, L. Molecular and biochemical analysis of the galactose phenotype of dairy Streptococcus thermophilus strains reveals four different fermentation profiles. J. Appl. Microbiol. 2005, 71, 3659–3667.
43. Mukherjee, K.K. Isolation of galactose-fermenting thermophilic cultures and their use in the manufacture of low browning Mozzarella cheese. J. Dairy Sci. 1994, 77, 2839–2849.
44. Giraffa, G.; Paris, A.; Valcavi, L.; Gatti, M.; Neviani, E. Genotypic and phenotypic heterogeneity of Streptococcus thermophilus strains isolated from dairy products. J. Appl. Microbiol. 2001, 91, 937–943.
45. Mora, D.; Fortina, M.G.; Parini, C.; Ricci, G.; Gatti, M.; Giraffa, G.; Manachini, P.L. Genetic diversity and technological properties of Streptococcus thermophilus strains isolated from dairy products. J. Appl. Microbiol. 2002, 93, 278–287.
46. Morandi, S.; Brasca, M. Safety aspects, genetic diversity and technological characterisation of wild-type Streptococcus thermophilus strains isolated from north Italian traditional cheeses. Food Control 2012, 23, 203–209.
47. Erkus, O.; Okuklu, B.; Yenidunya, A.F.; Harsa, S. High genetic and phenotypic variability of Streptococcus thermophilus strains isolated from artisanal Yuruk yoghurts. LWT-Food Sci. Technol. 2014, 58, 348–354.
48. Thomas, M.; Wrzosek, L.; Ben-Yahia, L.; Noordine, M.-L.; Gitton, C.; Chevret, D.; Langella, P.; Mayeur, C.; Cherbuy, C.; Rul, F. Carbohydrate metabolism is essential for the colonization of Streptococcus thermophilus in the digestive tract of gnotobiotic rats. PLoS ONE 2011, 6, e28789.
49. Maxwell, E.S.; Kurahasi, K.; Kalckar, H.M. Enzymes of the Leloir pathway. Methods Enzymol. 1962, 5, 174–189.
50. Vaughan, E.E.; van den Bogaard, P.T.; Catzeddu, P.; Kuipers, O.P.; de Vos, W.M. Actiation of silent gal genes in the lac-gal regulon of Streptococcus thermophilus. J. Bacteriol. 2001, 183, 1184–1194.
51. Vaillancourt, K.; LeMay, J.D.; Lamoureux, M.; Frenette, M.; Moineau, S.; Vadeboncoeur, C. Characterization of a galactokinase-positive recombinant strain of Streptococcus thermophilus. Appl. Environ. Microbiol. 2004, 70, 4596–4603.
52. Van den Bogaard, R.T.C.; Hols, P.; Kuipers, O.P.; Kleerebezem, M.; de Vos, W.M. Sugar utilisation and conservation of the gal-lac gene cluster in Streptococcus thermophilus. Syst. Appl. Microbiol. 2004, 27, 10–17.
53. Anbukkarasi, K.; Nanda, D.K.; UmaMaheswari, T.; Hemalatha, T.; Singh, P.; Singh, R. Assessment of expression of Leloir pathway genes in wild-type galactose-fermenting Streptococcus thermophilus by real-time PCR. Eur. Food Res. Technol. 2014, 239, 895–903.
54. Sørensen, K.I.; Curic-Bawden, M.; Junge, M.P.; Janzen, T.; Johansen, E. Enhancing the sweetness of yoghurt through metabolic remodeling of carbohydrate metabolism in Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus. Appl. Environ. Microbiol. 2016, 82, 3683–3692.
55. Levander, F.; Rådström, P. Requirement for phosphoglucomutase in exopolysaccharide biosynthesis in glucose-and lactose-utilizing Streptococcus thermophilus. Appl. Environ. Microbiol. 2001, 67, 2734–2738.
56. Levander, F.; Svensson, M.; Rådström, P. Enhanced exopolysaccharide production by metabolic engineering of Streptococcus thermophilus. Appl. Environ. Microbiol. 2002, 68, 784–790.
57. Hirasuka, Y.; Li, G. Alcohol and eye diseases: A review of epidemiologic studies. J. Stud. Alcohol. 1992, 62, 372–402.
58. Broadbent, J.R.; McMahon, D.J.; Welker, D.L.; Oberg, C.J.; Moineau, S. Biochemistry, genetics, and applications of exopolysaccharide production in Streptococcus thermophilus: A review. J. Dairy Sci. 2003, 86, 407–423.
59. Hassan, A.N.; Frank, J.F.; Schmidt, K.A.; Shalab, S.I. Rheological properties of yogurt made with encapsulated non ropy lactic cultures. J. Dairy Sci. 1996, 79, 2091–2097.
60. Bhaskaracharya, R.K.; Shah, N.P. Texture characteristics and microstructure of skim milk mozzarella cheeses made using exopolysaccharide or non-exopolysaccharide producing starter cultures. Aust. J. Dairy Technol. 2000, 55, 132–138.
61. Amatayakul, T.; Sherkat, F.; Shah, N.P. Syneresis in set yogurt as affected by EPS starter cultures and levels of solids. Int. J. Dairy Technol. 2006, 59, 216–221.
62. Purwandari, U.; Shah, N.P.; Vasiljevic, T. Effects of exopolysaccharide producing strains of Streptococcus thermophilus on technological and rheological properties of set-type yoghurt. Int. Dairy J. 2007, 17, 1344–1352.
63. Marcial, G.; Messing, J.; Menchicchi, B.; Goycoolea, F.M.; Faller, G.; de Valdez Graciela, F.; Hensel, A. Effects of polysaccharide isolated from Streptococcus thermophilus CRL1190 on human gastric epithelial cells. Int. J. Biol. Macromol. 2013, 62, 217–224.
64. Ren, W.; Xia, Y.; Wang, G.; Zhang, H.; Zhu, S.; Ai, L. Bioactive exopolysaccharides from a S. thermophilus strain: Screening, purification and characterization. Int. J. Biol. Macromol. 2016, 86, 402–407.
65. Rodríguez, C.; Medici, M.; Mozzi, F.; de Valdez Graciela, F. Therapeutic effect of Streptococcus thermophilus CRL 1190-fermented milk on chronic gastritis. World J. Gastroenterol. 2010, 16, 1622–1630.
66. Ruas-Madiedo, P.; Abraham, A.; Mozzi, F.; Los Reyes-Gavilán, C.G.D. Functionality of exopolysaccharides produced by lactic acid bacteria. In Molecular Aspects of Lactic Acid Bacteria for Traditional and New Applications; Mayo, B., López, P., Pérez-Martínez, G., Eds.; Research Signpost: Kerala, India, 2008; pp. 137–166.
67. Laws, A.; Gu, Y.C.; Marshall, V. Biosynthesis, characterisation and design of bacterial exopolysaccharides from lactic acid bacteria. Biotechnol. Adv. 2001, 19, 597–625.
68. Zhang, J.; Cao, Y.; Wang, J.; Guo, X.; Zheng, Y.; Zhao, W.; Mei, X.; Guo, T.; Yang, Z. Physicochemical characteristics and bioactivities of the exopolysaccharide and its sulphated polymer from Streptococcus thermophilus GST-6. Carbohydr. Polym. 2016, 146, 368–375.
69. Mozzi, F.; Vaningelgem, F.; Hebert, E.M.; Meulen, R.V.D.; Moreno, M.R.F.; Valdez, G.F.D.; Vuyst, L.D. Diversity of heteropolysaccharide-producing lactic acid bacterium strains and their biopolymers. Appl. Environ. Microbiol. 2006, 72, 4431–4435.
70. Jolly, L.; Stingele, F. Molecular organization and functionality of exopolysaccharide gene clusters in lactic acid bacteria. Int. Dairy J. 2001, 11, 733–745.
71. Stingele, F.; Neeser, J.R.; Mollet, B. Identification and characterization of the eps (exopolysaccharide) gene cluster from Streptococcus thermophilus Sfi6. J. Bacteriol. 1996, 178, 1680–1690.
72. Kranenburg, R.V.; Marugg, J.D.; Swam, I.I.V.; Willem, N.J.; Devos, W.M. Molecular characterization of the plasmid encoded eps gene cluster essential for exopolysaccharide biosynthesis in Lactococcus lactis. Mol. Microbiol. 1997, 24, 387–397.
73. Bourgoin, F.; Pluvinet, A.; Gintz, B.; Decaris, B.; Guédon, G. Are horizontal transfers involved in the evolution of the Streptococcus thermophilus exopolysaccharide synthesis loci?. Gene 1999, 233, 151–161.
74. Stingele, F.; Vincent, S.J.F.; Faber, E.J.; Newell, J.W.; Kamerling, J.P.; Neeser, J.R. Introduction of the exopolysaccharide gene cluster from Streptococcus thermophilus, Sfi6 into Lactococcus lactis, MG1363: Production and characterization of an altered polysaccharide. Mol. Microbiol. 1999, 32, 1287–1295.
75. Van Kranenburg, R.; Vos, H.R.; Swam, I.I.V.; Kleerebezem, M.; de Vos, W.M. Functional analysis of glycosyltransferase genes from Lactococcus lactis and other gram-positive cocci: Complementation, expression, and diversity. J. Bacteriol. 1999, 181, 6347–6353.
76. Ruas-Madiedo, P.; Los Reyes-Gavilán, C.G.D. Invited Review: Methods for the screening, isolation, and characterization of exopolysaccharides produced by lactic acid bacteria. J. Dairy Sci. 2005, 88, 843–856.
77. Zisu, B.; Shah, N.P. Effects of pH, temperature, supplementation with whey protein concentrate, and adjunct cultures on the production of exopolysaccharides by Streptococcus thermophilus 1275. J. Dairy Sci. 2003, 86, 3405–3415.
78. Amatayakul, T.; Sherkat, F.; Shah, N.P. Physical characteristics of set yoghurt made with altered casein to whey protein ratios and EPS-producing starter cultures at 9 and 14% total solids. Food Hydrocoll. 2006, 20, 314–324.
79. Zisu, B.; Shah, N.P. Low-fat mozzarella as influenced by microbial exopolysaccharides, preacidification, and whey protein concentrate. J. Dairy Sci. 2005, 88, 1973–1985.
80. Degeest, B.; Vaningelgem, F.; Vuyst, L.D. Microbial physiology fermentation kinetics, and process engineering of heteropolysaccharide production by lactic acid bacteria. Int. Dairy J. 2001, 11, 747–757.
81. Li, D.; Li, J.; Zhao, F.; Wang, G.H.; Qin, Q.Q.; Hao, Y.L. The influence of fermentation condition on production and molecular mass of EPS produced by Streptococcus thermophilus 05–34 in milk-based medium. Food Chem. 2016, 197, 367–372.
82. Pébay, M.; Colmin, C.; Guédon, G.; Simonet, J.M.; Decaris, B. Chromosomal genetic instability in S. thermophilus. Lait Dairy Sci. Technol. 1993, 73, 181–190.
83. Savijoki, K.; Ingmer, H.; Varmanen, P. Proteolytic systems of lactic acid bacteria. Appl. Microbiol. Biotechnol. 2006, 71, 394–406.
84. Christensen, J.E.; Dudley, E.G.; Pederson, J.A.; Steele, J.L. Peptidases and amino acid catabolism in lactic acid bacteria. Antonie Van Leeuwenhoek 1999, 76, 217–246.
85. Shihata, A.; Shah, N.P. Proteolytic profiles of yogurt and probiotic bacteria. Int. Dairy J. 2000, 10, 401–408.
86. Liu, M.J.; Bayjanov, J.R.; Renckens, B.; Nauta, A.; Siezen, R.J. The proteolytic system of lactic acid bacteria revisited: A genomic comparison. BMC Genom. 2010, 11, 1–15.
87. Settachaimongkon, S.; Nout, M.J.R.; Fernandes, E.C.A.; Hettinga, K.A.; Vervoort, J.M.; van Hooijdonk, T.C.M.; Zwietering, M.H.; Smid, E.J.; van Valenberg, H.J.F. Influence of different proteolytic strains of Streptococcus thermophilus in co-culture with Lactobacillus delbrueckii subsp. bulgaricus on the metabolite profile of set-yoghurt. Int. J. Food Microbiol. 2014, 177, 29–36.
88. Chang, O.K.; Perrin, C.; Galia, W.; Saulnier, F.; Miclo, L.; Roux, E.; Driou, A.; Humbert, G.; Dary, A. Release of the cell-envelope protease PrtS in the growth medium of Streptococcus thermophilus 4F44. Int. Dairy J. 2012, 23, 91–98.
89. Shahbal, S.; Hemme, D.; Desmazeaud, M. High cell wall-associated proteinase activity of some Streptococcus thermophilus strains (H-strains) correlated with a high acidification rate in milk. Le Lait 1991, 71, 351–357.
90. Mora, D.; Ricci, G.; Guglielmetti, S.; Daffonchio, D.; Fortina, M.G. 16S–23S rRNA intergenic spacer region sequence variation in Streptococcus thermophilus and related dairy streptococci and development of a multiplex ITS-SSCP analysis for their identification. Microbiology 2003, 149, 807–813.
91. Cheng, H. Volatile flavor compounds in yogurt: A review. Crit. Rev. Food Sci. Nutr. 2010, 50, 938–950.
92. Ott, A.; Fay, L.B.; Chaintreau, A. Determination and origin of the aroma impact compounds of yogurt flavor. J. Agric. Food Chem. 1997, 45, 850–858.
93. Imhof, R.; Bosset, J.O. Relationships between microorganisms and formation of aroma compounds in fermented dairy products. Z. Lebensm. Unters. Forsch. 1994, 198, 267–276.
94. Liu, M.J.; Nauta, A.; Francke, C.; Siezen, R.J. Comparative genomics of enzymes in flavor-forming pathways from amino acids in lactic acid bacteria. Appl. Environ. Micobol. 2008, 74, 4590–4600.
95. Yvon, M.; Rijnen, L. Cheese flavour formation by amino acid catabolism. Int. Dairy J. 2001, 11, 185–201.
96. Smit, G.; Smit, B.A.; Engels, W.J.M. Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol. Rev. 2005, 29, 591–610.
97. Ardo, Y. Flavour formation by amino acid catabolism. Biotechnol. Adv. 2006, 24, 238–242.
98. Helinck, S.; Le Bars, D.; Moreau, D.; Yvon, M. Ability of thermophilic lactic acid bacteria to produce aroma compounds from amino acids. Appl. Environ. Micobol. 2004, 70, 3855–3861.
99. Akyol, I.; Ozcelik, F.G.; Karakas-Sen, A.; Ozkose, E.; Gezginc, Y.; Ekinci, M.S. Cloning and over expression of the als, pflA, and adhB genes in Streptococcus thermophilus and their effects on metabolite formation. Mol. Biotechnol. 2015, 57, 923–930.
100. Liu, W.J. Characteristics of Acid and Flavor-Producing Stretococcus thermophilus and Lactobacillus bulgaricus, as well as Their Functional Gene Typing and Expression. Ph.D. Thesis, Inner Mongolia Agricultural University, Hohhot, China, 2014.
101. Liu, W.J.; Yu, J.; Sun, Z.H.; Song, Y.Q.; Wang, X.N.; Wang, H.M.; Wuren, T.Y.; Zha, M.S.; Menghe, B.; Zhang, H.P. Relationships between functional genes in Lactobacillus delbrueckii ssp. bulgaricus isolates and phenotypic characteristics associated with fermentation time and flavor production in yogurt elucidated using multilocus sequence typing. J. Dairy Sci. 2016, 99, 89–103.
102. Turgeon, N.; Frenette, M.; Moineau, S. Characterization of a _-replicating plasmid from Streptococcus thermophilus. Plasmid 2004, 51, 24–36.
103. Solaiman, D.K.; Somkuti, G.A. Characterization of a novel Streptococcus thermophilus rolling-circle plasmid used for vector construction. Appl. Microbiol. Biotechnol. 1998, 50, 174–180.
104. Somkuti, G.A.; Steinberg, D.H. Molecular organization of plasmid pER13 in Streptococcus thermophilus. Biotechnol. Lett. 2007, 29, 1991–1999.