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Proteolytic System of Streptococcus thermophilus

  • Rodriguez-Serrano, G.M. (Departamento de Biotecnologia Universidad Autonoma Metropolitana-Iztapalapa) ;
  • Garcia-Garibay, M. (Departamento de Biotecnologia Universidad Autonoma Metropolitana-Iztapalapa) ;
  • Cruz-Guerrero, A.E. (Departamento de Biotecnologia Universidad Autonoma Metropolitana-Iztapalapa) ;
  • Gomez-Ruiz, L. (Departamento de Biotecnologia Universidad Autonoma Metropolitana-Iztapalapa) ;
  • Ayala-Nino, A. (Centro de Investigaciones Quimicas, Universidad Autonoma del Estado de Hidalgo) ;
  • Castaneda-Ovando, A. (Centro de Investigaciones Quimicas, Universidad Autonoma del Estado de Hidalgo) ;
  • Gonzalez-Olivares, L.G. (Centro de Investigaciones Quimicas, Universidad Autonoma del Estado de Hidalgo)
  • Received : 2018.07.10
  • Accepted : 2018.08.27
  • Published : 2018.10.28

Abstract

The growth of lactic acid bacteria (LAB) generates a high number of metabolites related to aromas and flavors in fermented dairy foods. These microbial proteases are involved in protein hydrolysis that produces necessary peptides for their growth and releases different molecules of interest, like bioactive peptides, during their activity. Each genus in particular has its own proteolytic system to hydrolyze the necessary proteins to meet its requirements. This review aims to highlight the differences between the proteolytic systems of Streptococcus thermophilus and other lactic acid bacteria (Lactococcus and Lactobacillus) since they are microorganisms that are frequently used in combination with other LAB in the elaboration of fermented dairy products. Based on genetic studies and in vitro and in vivo tests, the proteolytic system of Streptococcus thermophilus has been divided into three parts: 1) a serine proteinase linked to the cellular wall that is activated in the absence of glutamine and methionine; 2) the transport of peptides and oligopeptides, which are integrated in both the Dpp system and the Ami system, respectively; according to this, it is worth mentioning that the Ami system is able to transport peptides with up to 23 amino acids while the Opp system of Lactococcus or Lactobacillus transports chains with less than 13 amino acids; and finally, 3) peptide hydrolysis by intracellular peptidases, including a group of three exclusive of S. thermophilus capable of releasing either aromatic amino acids or peptides with aromatic amino acids.

Keywords

References

  1. Savijoki K, Ingmer H, Varmanen P. 2006. Proteolytic systems of lactic acid bacteria. Appl. Microbiol. Biotechnol. 71: 394-406. https://doi.org/10.1007/s00253-006-0427-1
  2. Rojas-Ronquillo A, Cruz-Guerrero A, Flores-Najera A, Rodriguez-Serrano G, Gomez-Ruiz L, Reyes-Grajeda JP, et al. 2012. Antithrombotic and angiotensin-converting enzyme inhibitory properties of peptides released from bovine casein by Lactobacillus casei Shirota. Food Biotech. 26: 1-8. https://doi.org/10.1080/08905436.2011.617252
  3. Kunji ERS, Mierau I, Hagting A, Poolman B, Konings WN. 1996. The proteolytic system of lactic acid bacteria. Antonie Van Leewenhoek 70: 187-221. https://doi.org/10.1007/BF00395933
  4. Liu M, Bayjanov JR, Renckens B, Nauta A, Siezen RJ. 2010. The proteolytic system of lactic acid bacteria revisited: a genomic comparison. BMC Genomics 297: 164-172.
  5. Gasson MJ, de Vos WM. 1994. The proteolytic system of lactic acid bacteria, pp. 169-210. In Gasson MJ, Vos WM (eds.), Genetics and Biotechnology of Lactic Acid Bacteria, Springer, Netehrlands.
  6. Chopin A. 1993. Organization and regulation of genes for amino acid biosynthesis in lactic acid bacteria. FEMS Microbiol. Rev. 12: 21-37. https://doi.org/10.1111/j.1574-6976.1993.tb00011.x
  7. Leroy F, DeVuyst L. 2004. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 15: 67-78. https://doi.org/10.1016/j.tifs.2003.09.004
  8. Letort C, Nardi M, Garault P, Monnet V, Juillard V. 2002. Casein utilization by Streptococcus thermophilus results in a diauxic growth in milk. Appl. Environ. Microbiol. 68: 3162-3165. https://doi.org/10.1128/AEM.68.6.3162-3165.2002
  9. Monnet C, Mora D, Corrieu G. 2005. Glutamine synthesis is essential for growth of Streptococcus thermophilus in milk and is linked to urea catabolism. Appl. Environ. Microbiol. 71: 3376-3378. https://doi.org/10.1128/AEM.71.6.3376-3378.2005
  10. Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N, et. al 2005. New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol. Rev. 29: 435-463.
  11. Herve-Jimenez L, Guillouard I, Guedon E, Gautier C, Boudebbouze S, Hols P, et. al 2008. Physiology of Streptococcus thermophilus during the late stage of milk fermentation with special regard to sulfur amino-acid metabolism. Proteomics 8: 4273-4286. https://doi.org/10.1002/pmic.200700489
  12. Letort C, Juillard V. 2001. Development of a minimal chemically-defined medium for the exponential growth of Streptococcus thermophilus. J. Appl. Microbiol. 91: 1023-1029 https://doi.org/10.1046/j.1365-2672.2001.01469.x
  13. Juille O, Le Bars D, Juillard V. 2005. The specificity of oligopeptide transport by Streptococcus thermophilus resembles that of Lactococcus lactis and not that of pathogenic streptococci. Microbiology 151: 1987-1994. https://doi.org/10.1099/mic.0.27730-0
  14. Motoshima H, Shiraishi T, Tsukasaki F, Kaminogawa S. 2003. Purification, characterization and gene cloning of lysil aminopeptidase from Streptococcus thermophilus YRC001. Biosci. Biotechnol. Biochem. 67: 772.782. https://doi.org/10.1271/bbb.67.772
  15. Zhang Q, Ren J, Zhao M, Zhao H, Regenstein JM, LiY, Wu J. 2011. Isolation and characterization of three novel peptides from casein hydrolysates that stimulate the growth of mixed cultures of Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus. J. Agric. Food Chem. 59: 7045-7053. https://doi.org/10.1021/jf200903u
  16. Dandoy D, Fremaux C, Henry-Frahan M, Horvath P, Boyaval P, Hols P, et al. 2011. The fast milk acidifying phenotype of Streptococcus thermophilus can be acquired by natural transformation of the genomic island encoding the cell-envelope proteinase PrtS. Microb. Cell Fact. 10: S21 https://doi.org/10.1186/1475-2859-10-S1-S21
  17. Pritchard GG, Coolbear, T. 1993. The physiology and biochemistry of the proteolytic system in lactic acid bacteria. FEMS Microbiol. Rev. 12: 179-206. https://doi.org/10.1111/j.1574-6976.1993.tb00018.x
  18. Poolman B, Kunji ERS, Hagting A, Juillard V, Konings WN. 1995. The proteolytic pathway of Lactococcus lactis. Soc. Appl. Bacteriol. Symp. Ser. 24: 65S-75S
  19. Fernand ez-Espla MD, Garault P, Monnet V, Rul F. 2000. Streptococcus thermophilus cell anchored proteinase: release, purification and biochemical and genetic characterization. Appl. Environ. Microbiol. 66: 4772-4778. https://doi.org/10.1128/AEM.66.11.4772-4778.2000
  20. Chang OK, Roux E, Awussi AA, Miclo L, Jardin J, Jameh N, et al. 2014. Use of a free form of the Streptococcus thermophilus cell envelope protease PrtS as a tool to produce bioactive peptides Int. Dairy J. 38: 104-115. https://doi.org/10.1016/j.idairyj.2014.01.008
  21. Laan H, Konings WN. 1989. The mechanism of proteinase release from Lactococcus lactis subsp. cremoris Wg2. Appl. Environ. Microbiol. 55: 3101-3106
  22. Yamamoto N, Aquino A, Takano T. 1993. Purification and specificity of a cell-wall-associated proteinase from Lactobacillus helveticus CP790. J. Biochem. 114: 740-745. https://doi.org/10.1093/oxfordjournals.jbchem.a124247
  23. Shihata A, Shah NP. 2000. Proteolytic profiles of yogurt and probiotic bacteria. Int. Dairy J. 10: 401-408. https://doi.org/10.1016/S0958-6946(00)00072-8
  24. Juillard V, Laan H, Kunji ERS, Jeronimus-Stratingh CM, Bruins AP, Konings WN. 1995. The extracellular PI-type proteinase of Lactococcus lactis hydrolyzes $\beta$-casein into more than one hundred different oligopeptides. J. Bacteriol. 12: 3472-3478.
  25. Renault PG, Corthier N, Goupil C, Delorme C, Ehrlich SD. 1996. Plasmid vectors from Gram-positive bacteria switching from high low copy number. Gene 12: 175-182.
  26. Courti P, Monnet V, Rull F. 2002. Cell-wall proteinases PrtS and PrtB have a different role in Streptococcus thermophilus/Lactobacillus bulgaricus mixed cultures in milk. Microbiology 148: 3413-3421. https://doi.org/10.1099/00221287-148-11-3413
  27. Chang OK, Perrin C, Galia W, Saulnier F, Miclo L, Roux E, et al. 2012. Release of the cell-envelope protease PrtS in the growth medium of Streptococcus thermophilus 4F44. Int. Dairy J. 148: 3413-3421.
  28. Somkuti GA, Paul M. 2010. Enzymatic fragmentation of the antimicrobial peptides casocidin and isracidin by Streptococcus thermophilus and Lactobacillus delbrueckii ssp. Bulgaricus. Appl. Microbiol. Biotechnol. 87: 235-242. https://doi.org/10.1007/s00253-009-2433-6
  29. Kunji ERS, Hagting A, DeVries CJ, Juillard V, Haandrikman AJ, Poolman B, et al. 1995. Transport of $\beta$-casein-derived peptides by the oligopeptide transport system is a crucial step in the proteolytic pathway of Lactococcus lactis. J. Biol. Chem. 27: 1569-1574.
  30. Mukhopadhya A, Noronha N, Bahar B, Ryan BA, Kelly PM, O'Loughlin IB, et al. 2014. Anti-inflammatory effects of a casein hydrolysate and its peptide-enriched fractions on $TNF{\alpha}$-challenged Caco-2 cells and LPS-challenged porcine colonic explants. Food Sci. Nutr. 2:712-723. https://doi.org/10.1002/fsn3.153
  31. Monnet V, Ley JP, Gonzalez S. 1992. Substrate specificity of the cell enveloped-located proteinase of Lactococcus lactis subsp lactis NCDO763. Int. J. Biochem. 24: 707-718. https://doi.org/10.1016/0020-711X(92)90004-K
  32. 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: 451-460. https://doi.org/10.1128/AEM.01018-09
  33. Exterkate FA, Alting AC, Bruinenberg PG. 1993. Diversity of cell envelope proteinase specificity among strain of Lactococcus lactis and its relationship to charge characteristics of the substrate-binding region. Appl. Environ. Microbiol. 59: 3640-3647.
  34. Hafezz Z, Cakir-Kiefer C, Girardet JM, Lecomte X, Galia W, Dary A, et al. 2015. New insights into the proteolytic system of Streptococcus thermophilus: use of Isracidin to characterize cell-associated extracellular peptidase activities. J. Agric. Food Chem. 63: 7522-7531. https://doi.org/10.1021/acs.jafc.5b01647
  35. Thomas S, Besset C, Courtin P, Rul F. 2010. The role of aminopeptidase PepS in the growth of Streptococcus thermophilus is not restricted to nitrogen nutrition. J. Appl. Microbiol. 108: 148-157. https://doi.org/10.1111/j.1365-2672.2009.04400.x
  36. Galia W, Perrin C, Genay M, Dary A. 2009. Variability and molecular typing of Streptococcus thermophilus strains displaying different proteolytic and acidifying properties. Int. Dairy. J. 19: 89-95. https://doi.org/10.1016/j.idairyj.2008.08.004
  37. Galia W, Jameh N, Perrin C, Genay M, Dary-Mourot A. 2016. Acquisition of PrtS in Streptococcus thermophilus is not enough in certain strains to achieve rapid milk acidification. Diary Sci. Technol. 96: 623-636. https://doi.org/10.1007/s13594-016-0292-3
  38. Tian H, Li B, Evivie SE, Sarker SK, Chowdhury S, Lu J, et al. 2018. Technological and genomic analysis of roles of the cell-envelope protease PrtS in yoghurt starter development. Int. J. Mol. Sci. 19: 1068-1085. https://doi.org/10.3390/ijms19041068
  39. Bassi D, Cappa F, Gazzola S, Orrù L, Cocconcelli PS. 2017. Biofilm formation on stainless steel by Streptococcus thermophilus UC8547 in milk environments is mediated by the proteinase PrtS. Appl. Environ. Microbiol. 83: 1-12.
  40. Akpemado KM, Bracquart PA. 1983. Uptake of branched-chain amino acids by Streptococcus thermophilus. Appl. Environ. Microbiol. 45: 136-140.
  41. Heefner DL, Harold FM. 1982. ATP-driven sodium pump in Streptococcus faecalis. Proc. Nati. Acad. Sci. USA 79: 2798-2802. https://doi.org/10.1073/pnas.79.9.2798
  42. Podbielski A, Bettina ABL. 1998. The group A streptococcal dipeptide permease (Dpp) is involved in the uptake of essential amino acids and affects the expression of cysteine protease. Mol. Microbiol. 28: 1323-1334. https://doi.org/10.1046/j.1365-2958.1998.00898.x
  43. Doeven MK, Kok J, Poolman B. 2005. Specificity and selectivity determinants of peptide transport in Lactococcus lactis and other microorganisms. Mol. Microbiol. 57: 640-649. https://doi.org/10.1111/j.1365-2958.2005.04698.x
  44. Lamarque M, Charbonnel P, Aubel D, Piard JC, Atlan D, Juillard V. 2004. A multifunction ABC transporter (Opt) contributes to diversity of peptide uptake specificity within the genus Lactococcus. J. Bateriol. 186: 6492-6500.
  45. Garault P, Le Bars D, Besset C, Monnet V. 2002. Three oligopeptide-binding proteins are involved in the oligopeptide transport of Streptococcus thermophilus. J. Biol. Chem. 4: 32-39.
  46. Gardan R, Besset C, Guillot A, Gitton C, Monnet V. 2009.The oligopeptide transport system is essential for the development of natural competence in Streptococcus thermophilus strain LMD-9. J. Bacteriol. 14: 4647-4655.
  47. Gardan R, Besset C, Gitton C, Guillot A, Fontaine L, Hols P, et al. 2013. Extracellular life cycle of ComS, the competence-stimulating peptide of Streptococcus thermophilus. J. Bacteriol. 8: 1845-1855.
  48. Rul F, Monnet V. 1997. Presence of additional peptidases in Streptococcus thermophilus CNRZ 302 compared to Lactococcus lactis. J. Appl. Microbiol. 82: 695-704. https://doi.org/10.1046/j.1365-2672.1997.00185.x
  49. Rul F, Monnet V, Gripon JC. 1994. Purification and characterization of a general aminopeptidase (St-PepN) from Streptococcus salivarius subsp. thermophilus CNRZ302. J. Dairy Sci. 77: 2880-2889. https://doi.org/10.3168/jds.S0022-0302(94)77228-3
  50. Niven GW, Hold er SA, Stroman P. 1995. A stud y of the substrate specificity of aminopeptidase N from Lactococcus lactis subsp. cremoris Wg2. Appl. Microbiol. Biotechnol. 44: 100-105. https://doi.org/10.1007/BF00164487
  51. Chavagnat F, Casey MG, Meyer J. 1999. Purification, characterization, gene cloning, sequencing, and overexpression of aminopeptidase N from Streptococcus thermophilus A. Appl. Environ. Microbiol. 65: 3001-3007.
  52. Sieuwerts S, Molenaar D, van Hijum SAFT, Beerthuyzen M, Stevens MJA, Janssen PWM, et al. 2010. Mixed-culture transcriptome analysis reveals the molecular basis of mixed-culture growth in Streptococcus thermophilus and Lactobacillus bulgaricus. Appl. Environ. Microbiol. 76: 7775-7784. https://doi.org/10.1128/AEM.01122-10
  53. Tan PS, van Alen-Boerrigter IJ, Poolman B, Seizen RJ, de Vos WM, Konings WN. 1992. Characterization of the Lactococcus lactis papN gene encoding an aminopeptidase homologous to mammalian aminopeptidase N. FEBS Lett. 306: 9-16. https://doi.org/10.1016/0014-5793(92)80827-4
  54. Klein JR, Klein U, Schad M, Plapp R. 1993. Cloning DNA sequence analysis and partial characterization of pepN a lysis aminopeptidase from Lactobacillus delbrúckii subsp. Lactis DSM7290. Eur. J. Biochem. 217: 105-114 https://doi.org/10.1111/j.1432-1033.1993.tb18224.x
  55. Christensen JE, Lin D, Palva A, Steele JL. 1995. Sequence analysis, distribution and expression of an aminopeptidase N-encoding gene from Lactobacillus helveticus CNRZ32. Gene 155: 89-93 https://doi.org/10.1016/0378-1119(94)00924-H
  56. Chapot-Chartier MP, Rul F, Nardi M, Gripon JC. 1994. Gene cloning and characterization of PepC, a cysteine aminopeptidase from Streptococcus thermophilus, with sequence similarity to the eukaryotic bleomycin hydrolase. Eur. J. Biochem. 224: 497-506 https://doi.org/10.1111/j.1432-1033.1994.00497.x
  57. Motoshima H, Kaminagawa S. 2013. Aminopeptidase T, pp. 1674-1677. In Rawling, DN, Salvesen G (eds.), Handbook of Proteolytic Enzymes, 3rd Ed. Academic Press, California, USA.
  58. Fernandez-Espla MD, Rul F. 1999. PepS from Streptococcus thermophilus a new member of the aminopeptidaset family of thermophilic bacteria. Eur. J. Biochem. 263: 502-510. https://doi.org/10.1046/j.1432-1327.1999.00528.x
  59. Liu F, Du L, Du P, Huo G. 2009. Possible promoter regions within the proteolytic system in Streptococcus thermophilus and their interaction with the CodY homolog. FEMS Microbiol. Lett. 297: 164-172. https://doi.org/10.1111/j.1574-6968.2009.01672.x
  60. Simonen M, Palva I. 1993. Protein secretion in Bacillus species. Microbiol. Rev. 57: 109-137.
  61. Adda J, Gripon JC, Vassal L. 1982. The chemistry of flavour and texture development in cheese. Food Chem. 9: 115-129. https://doi.org/10.1016/0308-8146(82)90073-5
  62. Dunn HC, Lindsay RC. 1985. Evaluation of the role of microbial Strecker-derived aroma compounds in unclean-type flavours of Cheddar cheese. J. Dairy Sci. 68: 2859-2874. https://doi.org/10.3168/jds.S0022-0302(85)81179-6
  63. Lee CW, Desmazeaud MJ. 1985. Utilization of aromatic amino acids as nitrogen sources in Brevibacterium linens: an inducible aromatic amino acid aminotransferase. Arch. Microbiol. 140: 331-337. https://doi.org/10.1007/BF00446973
  64. Tsakalidou E, Anastasiou R, Papadimitriou K, Manolopoulou E, Kalantzopoulos G. 1997. Purification and characterisation of an intracellular X-prolyl-dipeptidyl aminopeptidase from Streptococcus thermophilus ACA-DC 4. J. Biotechnol. 59: 203-211.
  65. Anastasiou R, Papadelli M, Georgalaki MD, Kalantzopoulos G, Tsakalidou E. 2002. Cloning and sequencing of the gene encoding X-prolyl-dipeptidyl aminopeptidase (PepX) from Streptococcus thermophilus strain ACA-DC4. J. Appl. Microbiol. 93: 52-59. https://doi.org/10.1046/j.1365-2672.2002.01659.x
  66. Deutsch SM, Molle D, Gagnaire V, Piot M, Atlan D, Lortal S. 2000. Hydrolysis of sequenced $\beta$-casein peptides provides new insight into peptidase activity from thermophilic lactic acid bacteria and highlights intrinsic resistance of phosphopeptides. Appl. Environ. Microbiol. 12: 5360-5367.
  67. Meyer J, Jordi R. 1987. Purification and characterization of X-prolyl-dipeptidyl-aminopeptidase from Lactobacillus lactis and from Streptococcus thermophilus. J. Dairy Sci. 70: 738-745. https://doi.org/10.3168/jds.S0022-0302(87)80068-1
  68. Atlan D, Laloi P, Portalier R. 1990. X-prolyl-dipeptidyl aminopeptidase of Lactobacillus delbrueckii subsp. bulgaricus: characterization of the enzyme and isolation of deficient mutants. Appl. Environ. Microbiol. 56: 2174-2179. https://doi.org/10.1128/AEM.56.7.2174-2179.1990
  69. Khalid NM, Marth EH. 1990 Purification and characterization of prolyl-dipeptidyl aminopeptidase from Lactobacillus helveticus CNRZ32. Appl. Environ. Microbiol. 56: 381-388.
  70. Bockelmann W, Fobker M, Teuber M. 1991 Purification and characterisation of the X-prolyl-dipeptidyl-aminopeptidase from Lactobacillus delbrueckii subsp. bulgaricus and Lactobacillus acidophilus. Int. Dairy J. 1: 51-66. https://doi.org/10.1016/0958-6946(91)90027-6
  71. Giannoglou M, Alexandrakis Z, Stavros P, Katsaros G, Katapodis P, Nounesis G, et al, 2018. Effect of high pressure on modifications and enzymatic activity of a purified X-prolyl dipeptidyl aminopeptidase from Streptococcus thermophilus. Food Chem. 248: 304-311. https://doi.org/10.1016/j.foodchem.2017.12.037
  72. Chavagnat F, Meyer J, Casey MG. 2000. Purification, characterisation, cloning and sequencing of the gene encoding oligopeptidase PepO from Streptococcus thermophilus A. FEMS Microbiol Lett. 191: 79-85. https://doi.org/10.1111/j.1574-6968.2000.tb09322.x

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