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References

  1. Altermann, E., W. M. Russell, M. A. Azcarate-Peril, R. Barrangou, B. L. Buck, O. McAuliffe, et al. 2005. Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc. Natl. Acad. Sci. USA 102: 3906-3912.
    Pubmed PMC CrossRef
  2. Bolotin, A., B. Quinquis, P. Renault, A. Sorokin, S. D. Ehrlich, S. Kulakauskas, et al. 2004. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat. Biotechnol. 22: 1554-1558.
    Pubmed CrossRef
  3. Burton, J. P., P. A. Wescombe, C. J. Moore, C. N. Chilcott, and J. R. Tagg. 2006. Safety assessment of the oral cavity probiotic Streptococcus salivarius K12. Appl. Environ. Microbiol. 72:3050-3053.
    Pubmed PMC CrossRef
  4. Coenye, T. and P. Vandamme. 2003. Extracting phylogenetic information from whole-genome sequencing projects: The lactic acid bacteria as a test case. Microbiology 149: 3507-3517.
    Pubmed CrossRef
  5. Dave, R. I. 1991. Standardizing conditions for pilot scale production and storage of buffalo milk dahi using selected strains of Streptococcus thermophilus. Dissertation. Gujarat Agricultural University, S. K. Nagar, India.
  6. Dave, R. I., J. M. Dave, and S. S. Sannabhadti. 1993. Effect of starter culture and total solids on β-D-galactosidase activity during manufacture and storage of dahi. Indian J. Dairy Sci. 46: 544-546.
  7. Dave, R. I., J. M. Dave, and S. S. Sannabhadti. 1993. Microbial changes during manufacture and storage of buffalo milk dahi. J. Dairy. Foods Home Sci. 12: 83-88.
  8. Elli, M., M. L. Callegari, S. Ferrari, E. Bessi, D. Cattivelli, S. Soldi, et al. 2006. Survival of yogurt bacteria in the human gut. Appl. Environ. Microbiol. 72: 5113-5117.
    Pubmed PMC CrossRef
  9. Falentin, H., S. M. Deutsch, G. Jan, V. Loux, A. Thierry, S. Parayre, et al. 2010. The complete genome of Propionibacterium freudenreichii CIRM-BIA1, a hardy actinobacterium with food and probiotic applications. PLoS One 5: e11748.
    Pubmed PMC CrossRef
  10. Fath, M. J., H. K. Mahanty, and R. Kolter. 1989. Characterization of a purF operon mutation which affects colicin V production. J. Bacteriol. 171: 3158-3161.
    Pubmed PMC
  11. Garault, P., C. Letort, V. Juillard, and V. Monnet. 2000. Branched-chain amino acid biosynthesis is essential for optimal growth of Streptococcus thermophilus in milk. Appl. Environ. Microbiol. 66: 5128-5133.
    Pubmed PMC CrossRef
  12. Hao, P., H. Zheng, Y. Yu, G. Ding, W. Gu, S. Chen, et al. 2011. Complete sequencing and pan-genomic analysis of Lactobacillus delbrueckii subsp. bulgaricus reveal its genetic basis for industrial yogurt production. PLoS One 6: e15964.
    Pubmed PMC CrossRef
  13. Hiller, N. L., B. Janto, J. S. Hogg, R. Boissy, S. Yu, E. Powell, et al. 2007. Comparative genomic analyses of seventeen Streptococcus pneumoniae strains: Insights into the pneumococcal supragenome. J. Bacteriol. 189: 8186-8195.
    Pubmed PMC CrossRef
  14. Iyer, R., S. K. Tomar, S. Kapil, J. Mani, and S. Rameshwar. 2010. Probiotic properties of folate producing Streptococcus thermophilus strains. Food Res. Int. 43: 8.
    CrossRef
  15. Khalil, R. 2009. Evidence for probiotic potential of a capsularproducing Streptococcus thermophilus CHCC 3534 strain. Pol. J. Microbiol. 58: 49-55.
    Pubmed
  16. Klaenhammer, T. R., M. A. Azcarate-Peril, E. Altermann, and R. Barrangou. 2007. Influence of the dairy environment on gene expression and substrate utilization in lactic acid bacteria. J. Nutr. 137: 748S-750S.
    Pubmed
  17. Krastel, K., D. B. Senadheera, R. Mair, J. S. Downey, S. D. Goodman, and D. G. Cvitkovitch. 2010. Characterization of a glutamate transporter operon, glnQHMP, in Streptococcus mutans and its role in acid tolerance. J. Bacteriol. 192: 984993.
    Pubmed PMC CrossRef
  18. Kumar, R. 1990. Standardizing conditions for pilot scale production and storage of cow milk dahi using Streptococcus thermophilus strains as starter culture - some microbiological aspects. Dissertation. Gujarat Agricultural University, S. K. Nagar, India.
  19. Lebeer, S., J. Vanderleyden, and S. C. De Keersmaecker. 2008. Genes and molecules of lactobacilli supporting probiotic action. Microbiol. Mol. Biol. Rev. 72: 728-764.
    Pubmed PMC CrossRef
  20. Mayo, B., D. van Sinderen, and M. Ventura. 2008. Genome analysis of food grade lactic acid-producing bacteria: From basics to applications. Curr. Genomics 9: 169-183.
    Pubmed PMC CrossRef
  21. Pastink, M. I., B. Teusink, P. Hols, S. Visser, W. M. de Vos, and J. Hugenholtz. 2009. Genome-scale model of Streptococcus thermophilus LMG18311 for metabolic comparison of lactic acid bacteria. Appl. Environ. Microbiol. 75: 3627-3633.
    Pubmed PMC CrossRef
  22. Postma, P. W., J. W. Lengeler, and G. R. Jacobson. 1993. Phosphoenolpyruvate: Carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57: 543-596.
    Pubmed PMC
  23. Prajapati, J. B., C. D. Khedkar, J. Chitra, S. Suja, V. Mishra, V. Sreeja, et al. 2011. Whole-genome shotgun sequencing of an Indian-origin Lactobacillus helveticus strain, MTCC 5463, with probiotic potential. J. Bacteriol. 193: 4282-4283.
    Pubmed PMC CrossRef
  24. Prajapati, J. B., C. D. Khedkar, J. Chitra, S. Suja, V. Mishra, V. Sreeja, et al. 2012. Whole-genome shotgun sequencing of Lactobacillus rhamnosus MTCC 5462, a strain with probiotic potential. J. Bacteriol. 194: 1264-1265.
    Pubmed PMC CrossRef
  25. Rodionov, D. A. and M. S. Gelfand. 2005. Identification of a bacterial regulatory system for ribonucleotide reductases by phylogenetic profiling. Trends Genet. 21: 385-389.
    Pubmed CrossRef
  26. Roussel, Y., F. Bourgoin, G. Guedon, M. Pebay, and B. Decaris. 1997. Analysis of the genetic polymorphism between three Streptococcus thermophilus strains by comparing their physical and genetic organization. Microbiology 143 (Pt 4): 1335-1343.
    Pubmed CrossRef
  27. Salminen, S., J. Nurmi, and M. Gueimonde. 2005. The genomics of probiotic intestinal microorganisms. Genome Biol. 6: 225.
    Pubmed PMC CrossRef
  28. Saxena, A. 1990. Performance evaluation of Streptococcus thermophilus strains in skim milk dahi manufacture with reference to its microbiology and keeping quality. Dissertation. Gujarat Agricultural University, S. K. Nagar, India.
  29. Vinderola, C. G., P. Mocchiutti, and J. A. Reinheimer. 2002. Interactions among lactic acid starter and probiotic bacteria used for fermented dairy products. J. Dairy Sci. 85: 721-729.
    CrossRef
  30. Vogel, R. F., M. Pavlovic, M. A. Ehrmann, A. Wiezer, H. Liesegang, S. Offschanka, et al. 2011. Genomic analysis reveals Lactobacillus sanfranciscensis as stable element in traditional sourdoughs. Microb. Cell Fact 10 (Suppl 1): S6.
    Pubmed PMC CrossRef
  31. Xu, P., X. Ge, L. Chen, X. Wang, Y. Dou, J. Z. Xu, et al. 2011. Genome-wide essential gene identification in Streptococcus sanguinis. Sci. Rep. 1: 125.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2013; 23(4): 459-466

Published online April 28, 2013 https://doi.org/10.4014/jmb.1210.10030

Copyright © The Korean Society for Microbiology and Biotechnology.

Genomic Analysis of Dairy Starter Culture Streptococcus thermophilus MTCC 5461

Jashbhai B. Prajapati 1, Neelam M. Nathani 2, Amrutlal K. Patel 2, Suja Senan 1 and Chaitanya G. Joshi 2*

1Department of Dairy Microbiology, SMC College of Dairy Science, Anand Agricultural University, Anand-388 001, Gujarat, India, 2Department of Animal Biotechnology, College of Veterinary Science and Animal Husbandry, Anand Agricultural University, Anand-388 001, Gujarat, India

Received: October 12, 2012; Accepted: December 17, 2012

Abstract

The lactic acid bacterium Streptococcus thermophilus is
widely used as a starter culture for the production of
dairy products. Whole-genome sequencing is expected to
utilize the genetic basis behind the metabolic functioning
of lactic acid bacterium (LAB), for development of their
use in biotechnological and probiotic applications. We
sequenced the whole genome of Streptococcus thermophilus
MTCC 5461, the strain isolated from a curd source, by
454 GS-FLX titanium and Ion Torrent PGM. We performed
comparative genome analysis using the local BLAST and
RDP for 16S rDNA comparison and by the RAST server
for functional comparison against the published genome
sequence of Streptococcus thermophilus CNRZ 1066. The
whole genome size of S. thermophilus MTCC 5461 is of
1.73Mb size with a GC content of 39.3%. Streptococcal
virulence-related genes are either inactivated or absent in
the strain. The genome possesses coding sequences for
features important for a probiotic organism such as
adhesion, acid tolerance, bacteriocin production, and lactose
utilization, which was found to be conserved among the
strains MTCC 5461 and CNRZ 1066. Biochemical analysis
revealed the utilization of 17 sugars by the bacterium,
where the presence of genes encoding enzymes involved in
metabolism for 16 of these 17 sugars were confirmed in
the genome. This study supports the facts that the strain
MTCC 5461 is nonpathogenic and harbors essential
features that can be exploited for its probiotic potential.

Keywords: Streptococcus thermophilus, dairy, bioinformatics, genome analysis, coding sequences, fermentation profile

References

  1. Altermann, E., W. M. Russell, M. A. Azcarate-Peril, R. Barrangou, B. L. Buck, O. McAuliffe, et al. 2005. Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc. Natl. Acad. Sci. USA 102: 3906-3912.
    Pubmed KoreaMed CrossRef
  2. Bolotin, A., B. Quinquis, P. Renault, A. Sorokin, S. D. Ehrlich, S. Kulakauskas, et al. 2004. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat. Biotechnol. 22: 1554-1558.
    Pubmed CrossRef
  3. Burton, J. P., P. A. Wescombe, C. J. Moore, C. N. Chilcott, and J. R. Tagg. 2006. Safety assessment of the oral cavity probiotic Streptococcus salivarius K12. Appl. Environ. Microbiol. 72:3050-3053.
    Pubmed KoreaMed CrossRef
  4. Coenye, T. and P. Vandamme. 2003. Extracting phylogenetic information from whole-genome sequencing projects: The lactic acid bacteria as a test case. Microbiology 149: 3507-3517.
    Pubmed CrossRef
  5. Dave, R. I. 1991. Standardizing conditions for pilot scale production and storage of buffalo milk dahi using selected strains of Streptococcus thermophilus. Dissertation. Gujarat Agricultural University, S. K. Nagar, India.
  6. Dave, R. I., J. M. Dave, and S. S. Sannabhadti. 1993. Effect of starter culture and total solids on β-D-galactosidase activity during manufacture and storage of dahi. Indian J. Dairy Sci. 46: 544-546.
  7. Dave, R. I., J. M. Dave, and S. S. Sannabhadti. 1993. Microbial changes during manufacture and storage of buffalo milk dahi. J. Dairy. Foods Home Sci. 12: 83-88.
  8. Elli, M., M. L. Callegari, S. Ferrari, E. Bessi, D. Cattivelli, S. Soldi, et al. 2006. Survival of yogurt bacteria in the human gut. Appl. Environ. Microbiol. 72: 5113-5117.
    Pubmed KoreaMed CrossRef
  9. Falentin, H., S. M. Deutsch, G. Jan, V. Loux, A. Thierry, S. Parayre, et al. 2010. The complete genome of Propionibacterium freudenreichii CIRM-BIA1, a hardy actinobacterium with food and probiotic applications. PLoS One 5: e11748.
    Pubmed KoreaMed CrossRef
  10. Fath, M. J., H. K. Mahanty, and R. Kolter. 1989. Characterization of a purF operon mutation which affects colicin V production. J. Bacteriol. 171: 3158-3161.
    Pubmed KoreaMed
  11. Garault, P., C. Letort, V. Juillard, and V. Monnet. 2000. Branched-chain amino acid biosynthesis is essential for optimal growth of Streptococcus thermophilus in milk. Appl. Environ. Microbiol. 66: 5128-5133.
    Pubmed KoreaMed CrossRef
  12. Hao, P., H. Zheng, Y. Yu, G. Ding, W. Gu, S. Chen, et al. 2011. Complete sequencing and pan-genomic analysis of Lactobacillus delbrueckii subsp. bulgaricus reveal its genetic basis for industrial yogurt production. PLoS One 6: e15964.
    Pubmed KoreaMed CrossRef
  13. Hiller, N. L., B. Janto, J. S. Hogg, R. Boissy, S. Yu, E. Powell, et al. 2007. Comparative genomic analyses of seventeen Streptococcus pneumoniae strains: Insights into the pneumococcal supragenome. J. Bacteriol. 189: 8186-8195.
    Pubmed KoreaMed CrossRef
  14. Iyer, R., S. K. Tomar, S. Kapil, J. Mani, and S. Rameshwar. 2010. Probiotic properties of folate producing Streptococcus thermophilus strains. Food Res. Int. 43: 8.
    CrossRef
  15. Khalil, R. 2009. Evidence for probiotic potential of a capsularproducing Streptococcus thermophilus CHCC 3534 strain. Pol. J. Microbiol. 58: 49-55.
    Pubmed
  16. Klaenhammer, T. R., M. A. Azcarate-Peril, E. Altermann, and R. Barrangou. 2007. Influence of the dairy environment on gene expression and substrate utilization in lactic acid bacteria. J. Nutr. 137: 748S-750S.
    Pubmed
  17. Krastel, K., D. B. Senadheera, R. Mair, J. S. Downey, S. D. Goodman, and D. G. Cvitkovitch. 2010. Characterization of a glutamate transporter operon, glnQHMP, in Streptococcus mutans and its role in acid tolerance. J. Bacteriol. 192: 984993.
    Pubmed KoreaMed CrossRef
  18. Kumar, R. 1990. Standardizing conditions for pilot scale production and storage of cow milk dahi using Streptococcus thermophilus strains as starter culture - some microbiological aspects. Dissertation. Gujarat Agricultural University, S. K. Nagar, India.
  19. Lebeer, S., J. Vanderleyden, and S. C. De Keersmaecker. 2008. Genes and molecules of lactobacilli supporting probiotic action. Microbiol. Mol. Biol. Rev. 72: 728-764.
    Pubmed KoreaMed CrossRef
  20. Mayo, B., D. van Sinderen, and M. Ventura. 2008. Genome analysis of food grade lactic acid-producing bacteria: From basics to applications. Curr. Genomics 9: 169-183.
    Pubmed KoreaMed CrossRef
  21. Pastink, M. I., B. Teusink, P. Hols, S. Visser, W. M. de Vos, and J. Hugenholtz. 2009. Genome-scale model of Streptococcus thermophilus LMG18311 for metabolic comparison of lactic acid bacteria. Appl. Environ. Microbiol. 75: 3627-3633.
    Pubmed KoreaMed CrossRef
  22. Postma, P. W., J. W. Lengeler, and G. R. Jacobson. 1993. Phosphoenolpyruvate: Carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57: 543-596.
    Pubmed KoreaMed
  23. Prajapati, J. B., C. D. Khedkar, J. Chitra, S. Suja, V. Mishra, V. Sreeja, et al. 2011. Whole-genome shotgun sequencing of an Indian-origin Lactobacillus helveticus strain, MTCC 5463, with probiotic potential. J. Bacteriol. 193: 4282-4283.
    Pubmed KoreaMed CrossRef
  24. Prajapati, J. B., C. D. Khedkar, J. Chitra, S. Suja, V. Mishra, V. Sreeja, et al. 2012. Whole-genome shotgun sequencing of Lactobacillus rhamnosus MTCC 5462, a strain with probiotic potential. J. Bacteriol. 194: 1264-1265.
    Pubmed KoreaMed CrossRef
  25. Rodionov, D. A. and M. S. Gelfand. 2005. Identification of a bacterial regulatory system for ribonucleotide reductases by phylogenetic profiling. Trends Genet. 21: 385-389.
    Pubmed CrossRef
  26. Roussel, Y., F. Bourgoin, G. Guedon, M. Pebay, and B. Decaris. 1997. Analysis of the genetic polymorphism between three Streptococcus thermophilus strains by comparing their physical and genetic organization. Microbiology 143 (Pt 4): 1335-1343.
    Pubmed CrossRef
  27. Salminen, S., J. Nurmi, and M. Gueimonde. 2005. The genomics of probiotic intestinal microorganisms. Genome Biol. 6: 225.
    Pubmed KoreaMed CrossRef
  28. Saxena, A. 1990. Performance evaluation of Streptococcus thermophilus strains in skim milk dahi manufacture with reference to its microbiology and keeping quality. Dissertation. Gujarat Agricultural University, S. K. Nagar, India.
  29. Vinderola, C. G., P. Mocchiutti, and J. A. Reinheimer. 2002. Interactions among lactic acid starter and probiotic bacteria used for fermented dairy products. J. Dairy Sci. 85: 721-729.
    CrossRef
  30. Vogel, R. F., M. Pavlovic, M. A. Ehrmann, A. Wiezer, H. Liesegang, S. Offschanka, et al. 2011. Genomic analysis reveals Lactobacillus sanfranciscensis as stable element in traditional sourdoughs. Microb. Cell Fact 10 (Suppl 1): S6.
    Pubmed KoreaMed CrossRef
  31. Xu, P., X. Ge, L. Chen, X. Wang, Y. Dou, J. Z. Xu, et al. 2011. Genome-wide essential gene identification in Streptococcus sanguinis. Sci. Rep. 1: 125.
    Pubmed KoreaMed CrossRef