Stress Responses of Streptococci

  • José A. Lemos
  • Effie Tsakalidou
  • Konstantinos Papadimitriou
Part of the Food Microbiology and Food Safety book series (FMFS)


Streptococci belong to the lactic acid bacteria group and play a crucial role in the health of animals and humans. The genus compises mostly commensal species, including several opportunistic pathogens, or severe pathogens. In this chapter, streptococcal species are organized in groups according to their ecological niche, pathogenicity, and food compatibility because these are probably the key factors in driving the relevant stress physiology research. We initially focus on oral streptococci and the dental pathogen Streptococcus mutans, which is the best-studied species within the genus in terms of its stress responses. After that, we describe the stress behavior of the beta-hemolytic Lancefield’s group A and group B streptococci (i.e., Streptococcus pyogenes and Streptococcus agalactiae, respectively), as well as the nonbeta-hemolytic Streptococcus pneumoniae. The pathogenicity of these streptococci is clearly linked to their ability to turn on survival and stress responses against the host’s innate immunity. Finally, we concentrate on food-related streptococci, namely, Streptococcus thermophilus and Streptococcus macedonicus, which are primarily exposed to stresses related to food processing and storage. Throughout the chapter we attempt to highlight all areas in the field that have been scrutinized, as well as areas that deserve further investigation.


Lactic Acid Bacterium Acid Tolerance Bacteriocin Production Lactic Acid Bacterium Species Acid Adaptation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abranches J, Chen YY, Burne RA (2003) Characterization of Streptococcus mutans strains deficient in EIIAB Man of the sugar phosphotransferase system. Appl Environ Microbiol 69:4760–4769Google Scholar
  2. Abranches J, Candella MM, Wen ZT, Baker HV, Burne RA (2006) Different roles of EIIABMan and EIIGlc in regulation of energy metabolism, biofilm development, and competence in Streptococcus mutans. J Bacteriol 188:3748–3756Google Scholar
  3. Abranches J, Nascimento MM, Zeng, L, Browngardt, CM, Wen, ZT, Rivera MF, Burne RA (2008) CcpA regulates central metabolism and virulence gene expression in Streptococcus mutans. J Bacteriol 190:2340–2349Google Scholar
  4. Ahn SJ, Lemos JA, Burne RA (2005) Role of HtrA in growth and competence of Streptococcus mutans UA159. J Bacteriol 187:3028–3038Google Scholar
  5. Ahn SJ, Wen ZT, Burne RA (2006) Multilevel control of competence development and stress tolerance in Streptococcus mutans UA159. Infect Immun 74:1631–1642Google Scholar
  6. Ajdic D, McSham WM, McLaughlin RE, Savic G, Chang, J, Carson, MB, Primeaux C, Tian R, Kenton, S, Jia H, Lin S, Qian Y, Li S, Zhu H, Najar F, Lai H, White J, Roe BA, Ferretti JJ (2002) Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci USA 99:14434–14439Google Scholar
  7. Anastasiou R, Aktypis A, Georgalaki M, Papadelli M, De Vuyst L, Tsakalidou E (2009) Inhibition of Clostridium tyrobutyricum by Streptococcus macedonicus ACA–DC 198 under conditions mimicking Kasseri cheese production and ripening. Int Dairy J 19:330–335Google Scholar
  8. Andrus JM, Bowen SW, Klaenhammer TR, Hassan HM (2003) Molecular characterization and functional analysis of the manganese–containing superoxide dismutase gene (sodA) from Streptococcus thermophilus AO54. Arch Biochem Biophys 420:103–113Google Scholar
  9. Archibald FS, Fridovich I (1981) Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria. J Bacteriol 146:928–936Google Scholar
  10. Arena S, D’Ambrosio C, Renzone G, Rullo R, Ledda L, Vitale F, Maglione G, Varcamonti M, Ferrara L, Scaloni A (2006) A study of Streptococcus thermophilus proteome by integrated analytical procedures and differential expression investigations. Proteomics 6:181–192Google Scholar
  11. Auffray Y, Lecesne E, Hartke A, Boutibonnes P (1995) Basic features of the Streptococcus thermophilus heat shock response. Curr Microbiol 30:87–91Google Scholar
  12. Bates CS, Toukoki C, Neely MN, Eichenbaum Z (2005) Characterization of MtsR, a new metal regulator in group A Streptococcus, involved in iron acquisition and virulence. Infect Immun 73:5743–5753Google Scholar
  13. Bender GR, Sutton SV, Marquis RE (1986) Acid tolerance, proton permeabilities, and membrane ATPases of oral streptococci. Infect Immun 53:331–338Google Scholar
  14. Beres SB, Ritcher EW, Nagiec MJ, Sumby P, Porcella SF, DeLeo FR, Musser JM (2006) Molecular genetic anatomy of inter– and intraserotype variation in the human bacterial pathogen group A Streptococcus. Proc Natl Acad Sci USA 103:7059–7064Google Scholar
  15. Bernhardt J, Weibezahn J, Scharf C, Hecker M (2003) Bacillus subtilis during feast and famine: visualization of the overall regulation of protein synthesis during glucose starvation by proteome analysis. Genome Res 13:224–237Google Scholar
  16. Billroth T (1874) Untersuchungen uber die Vegetationsformen von Coccobacteria Septica [in German]. BerlinGoogle Scholar
  17. Biswas I, Drake L, Erkina D, Biswas S (2008) Involvement of sensor kinases in the stress tolerance response of Streptococcus mutans. J Bacteriol 190:68–77Google Scholar
  18. Biswas S, Biswas I (2005) Role of HtrA in surface protein expression and biofilm formation by Streptococcus mutans. Infect Immun 73:6923–6934Google Scholar
  19. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, Kulakauskas S, Lapidus A, Goltsman E, Mazur M, Pusch GD, Fonstein M, Overbeek R, Kyprides N, Purnelle B, Prozzi D, Ngui K, Masuy D, Hancy F, Burteau S, Boutry M, Delcour J, Goffeau A, Hols P (2004) Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat Biotechnol 22:1554–1558Google Scholar
  20. Booth IR (2002) Stress and the single cell: intrapopulation diversity is a mechanism to ensure survival upon exposure to stress. Int J Food Microbiol 78:19–30Google Scholar
  21. Borges F, Layec S, Thissebard A, Fernandez A, Gintz B, Hols P, Decaris B, Leblond-Bourget N (2005) cse, A chimeric and variable gene, encodes an extracellular protein involved in cellular segregation in Streptococcus thermophilus. J Bacteriol 187:2737–2746Google Scholar
  22. Bortoni ME, Terra VS, Hinds J, Andrew PW, Yesilkaya H (2009) The pneumococcal response to oxidative stress includes a role for Rgg. Microbiology 155:4123–4134Google Scholar
  23. Boyd DA, Cvitkovitch DG, Bleiweis AS, Kiriukhin MY, Debabov DV, Neuhaus FC, Hamilton IR (2000) Defects in D-alanyl-lipoteichoic acid synthesis in Streptococcus mutans results in acid sensitivity. J Bacteriol 182:6055–6065Google Scholar
  24. Brehm-Stecher BF, Johnson EA (2004) Single-cell microbiology: tools, technologies, and applications. Microbiol Mol Biol Rev 68:538–559Google Scholar
  25. Brenot A, King KY, Janowiak B, Griffith O, Caparon MG (2004) Contribution of glutathione peroxidase to the virulence of Streptococcus pyogenes. Infect Immun 72:408–413Google Scholar
  26. Brenot A, King KY, Caparon MG (2005) The PerR regulon in peroxide resistance and virulence of Streptococcus pyogenes. Mol Microbiol 55:221–234Google Scholar
  27. Brenot A, Weston BF, Caparon MG (2007) A PerR-regulated metal transporter (PmtA) is an interface between oxidative stress and metal homeostasis in Streptococcus pyogenes. Mol Microbiol 63:1185–1196Google Scholar
  28. Brown JS, Gilliland SM, Basavanna S, Holden DW (2004) phgABC, a three-gene operon required for growth of Streptococcus pneumoniae in hyperosmotic medium and in vivo. Infect Immun 72:4579–4588Google Scholar
  29. Caldas T, Laalami S, Richarme G (2000) Chaperone properties of bacterial elongation factor EF-G and initiation factor IF2. J Biol Chem 275:855–860Google Scholar
  30. Cao J, Chen D, Xu W, Chen T, Xu S, Luo J, Zhao Q, Liu B, Wang D, Zhang X, Shan Y, Yin Y (2007) Enhanced protection against pneumococcal infection elicited by immunization with the combination of PspA, PspC, and ClpP. Vaccine 25:4996–5005Google Scholar
  31. Cao J, Li D, Gong Y, Yin N, Chen T, Wong CK, Xu W, Luo J, Zhang X, Lam CW, Yin Y (2009) Caseinolytic protease: a protein vaccine which could elicit serotype-independent protection against invasive pneumococcal infection. Clin Exp Immunol 156:52–60Google Scholar
  32. Carapetis JR, Steer AC, Mulholland EK, Weber M (2005) The global burden of group A streptococcal diseases. Lancet Infect Dis 5:685–694Google Scholar
  33. Carlsson J (1983) Regulation of sugar metabolism in relation to feast-and-famine existence of plaque. In: Guggenheim B (Ed.), Cariology today. Karger, BaselGoogle Scholar
  34. Carmel-Harel O, Storz G (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54:439–461Google Scholar
  35. Casalta E, Montel MC (2008) Safety assessment of dairy microorganisms: the Lactococcus genus. Int J Food Microbiol 126:271–273Google Scholar
  36. Chang SK, Hassan HM (1997) Characterization of superoxide dismutase in Streptococcus thermophilus. Appl Environ Microbiol 63:3732–3735Google Scholar
  37. Charpentier E, Novak R, Tuomanen E (2000) Regulation of growth inhibition at high temperature, autolysis, transformation and adherence in Streptococcus pneumoniae by clpC. Mol Microbiol 37:717–726Google Scholar
  38. Chastanet A, Prudhomme M, Claverys JP, Msadek T (2001) Regulation of Streptococcus pneumoniae clp genes and their role in competence development and stress survival. J Bacteriol 183:7295–7307Google Scholar
  39. Chatfield CH, Koo H, Quivey RG Jr (2005) The putative autolysin regulator LytR in Streptococcus mutans plays a role in cell division and is growth-phase regulated. Microbiology 151:625–631Google Scholar
  40. Chattoraj P, Banerjee A, Biswas S, Biswas I (2010) ClpP of Streptococcus mutans differentially regulates expression of genomic islands, mutacin production, and antibiotic tolerance. J Bacteriol 192:1312–1323Google Scholar
  41. Chaussee MS, Phillips ER, Ferretti JJ (1997) Temporal production of streptococcal erythrogenic toxin B (streptococcal cysteine proteinase) in response to nutrient depletion. Infect Immun 65:1956–1959Google Scholar
  42. Chen PM, Chen HC, Ho CT, Jung CJ, Lien HT, Chen JY, Chia JS (2008) The two-component system ScnRK of Streptococcus mutans affects hydrogen peroxide resistance and murine macrophage killing. Microbes Infect 10:293–301Google Scholar
  43. Cheng Q, Campbell EA, Naughton AM, Johnson S, Masure HR (1997) The com locus controls genetic transformation in Streptococcus pneumoniae. Mol Microbiol 23:683–692Google Scholar
  44. Claverys JP, Prudhomme M, Martin B (2006) Induction of competence regulons as a general response to stress in gram-positive bacteria. Annu Rev Microbiol 60:451–475Google Scholar
  45. Claverys JP, Martin B, Havarstein LS (2007) Competence-induced fratricide in streptococci. Mol Microbiol 64:1423–1433Google Scholar
  46. Cochu A, Vadeboncoeur C, Moineau S, Frenette M (2003) Genetic and biochemical characterization of the phosphoenolpyruvate:glucose/mannose phosphotransferase system of Streptococcus thermophilus. Appl Environ Microbiol 69:5423–5432Google Scholar
  47. Cotter PD, Hill C (2003) Surviving the acid test: responses of Gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67:429–453Google Scholar
  48. Cotter PD, Gahan CG, Hill C (2000) Analysis of the role of the Listeria monocytogenes F0F1 -ATPase operon in the acid tolerance response. Int J Food Microbiol 60:137–146Google Scholar
  49. Cunningham MW (2000) Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13:470–511Google Scholar
  50. Dagkessamanskaia A, Moscoso M, Henard V, Guiral S, Overweg K, Reuter M, Martin B, Wells J, Claverys JP (2004) Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells. Mol Microbiol 51:1071–1086Google Scholar
  51. Dalton TL, Scott JR (2004) CovS inactivates CovR and is required for growth under conditions of general stress in Streptococcus pyogenes. J Bacteriol 186:3928–3937Google Scholar
  52. Davey HM, Kell DB (1996) Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analyses. Microbiol Rev 60:641–696Google Scholar
  53. De Angelis M, Gobbetti M (2004) Environmental stress responses in Lactobacillus: a review. Proteomics 4:106–122Google Scholar
  54. De Angelis M, Bini L, Pallini V, Cocconcelli PS, Gobbetti M (2001) The acid-stress response in Lactobacillus sanfranciscensis CB1. Microbiology 147:1863–1873Google Scholar
  55. De Vuyst L, Tsakalidou E (2008) Streptococcus macedonicus, a multi-functional and promising species for dairy fermentations. Int Dairy J 18:476–485Google Scholar
  56. Delorme C (2008) Safety assessment of dairy microorganisms: Streptococcus thermophilus. Int J Food Microbiol 126:274–277Google Scholar
  57. Deng DM, Liu MJ, ten Cate JM, Crielaard W (2007a) The VicRK system of Streptococcus mutans responds to oxidative stress. J Dent Res 86:606–610Google Scholar
  58. Deng DM, ten Cate JM, Crielaard W (2007b) The adaptive response of Streptococcus mutans towards oral care products: involvement of the ClpP serine protease. Eur J Oral Sci 115:363–370Google Scholar
  59. Derré I, Rapoport G, Msadek T (1999) CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria. Mol Microbiol 31:117–131Google Scholar
  60. Dunning DW, McCall LW, Powell WF, Arscott WT, McConocha EM, McClurg CJ, Goodman SD, Spatafora GA (2008) SloR modulation of the Streptococcus mutans acid tolerance response involves the GcrR response regulator as an essential intermediary. Microbiology 154:1132–1143Google Scholar
  61. Duwat P, Ehrlich SD, Gruss A (1995) The recA gene of Lactococcus lactis: characterization and involvement in oxidative and thermal stress. Mol Microbiol 17:1121–1131Google Scholar
  62. Edwards MS, Rench MA, Haffar AA, Murphy MA, Desmond MM, Baker CJ (1985) Long-term sequelae of group B streptococcal meningitis in infants. J Pediatr 106:717–722Google Scholar
  63. Eldholm V, Gutt B, Johnsborg O, Bruckner R, Maurer P, Hakenbeck R, Mascher T, Havarstein LS (2010) The pneumococcal cell envelope stress-sensing system LiaFSR is activated by murein hydrolases and lipid II-interacting antibiotics. J Bacteriol 192:1761–1773Google Scholar
  64. Facklam R (2002) What happened to the streptococci: overview of taxonomic and nomenclature changes. Clin Microbiol Rev 15:613–630Google Scholar
  65. Faustoferri RC, Hahn K, Weiss K, Quivey RG Jr (2005) Smx nuclease is the major, low-pH-inducible apurinic/apyrimidinic endonuclease in Streptococcus mutans. J Bacteriol 187:2705–2714Google Scholar
  66. Fernandez A, Borges F, Thibessard A, Gintz B, Decaris B, Leblond-Bourget N (2004a) Characterization of Streptococcus thermophilus CNRZ368 oxidative stress-resistant mutants: involvement of a potential Rgg-like transcriptional regulator. Lait 84:77–85Google Scholar
  67. Fernandez A, Thibessard A, Borges F, Gintz B, Decaris B, Leblond-Bourget N (2004b) Characterization of oxidative stress-resistant mutants of Streptococcus thermophilus CNRZ368. Arch Microbiol 182:364–372Google Scholar
  68. Ferrer M, Lunsdorf H, Chernikova TN, Yakimov M, Timmis KN, Golyshin PN (2004) Functional consequences of single:double ring transitions in chaperonins: life in the cold. Mol Microbiol 53:167–182Google Scholar
  69. Ferretti JJ, McShan WM, Ajdic D, Savic DJ, Savic G, Lyon, K, Primeaux C, Sezate S, Suvorov, AN, Kenton S, Lai HS, Lin SP, Qian Y, Jia HG, Najar FZ, Ren Q, Zhu H, Song L, White, J, Yuan X, Clifton SW, Roe, BA, McLaughlin R (2001) Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci USA 98:4658–4663Google Scholar
  70. Fozo EM, Quivey RG Jr (2004a) Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol 70:929–936Google Scholar
  71. Fozo EM, Quivey RG Jr (2004b) The fabM gene product of Streptococcus mutans is responsible for the synthesis of monounsaturated fatty acids and is necessary for survival at low pH. J Bacteriol 186:4152–4158Google Scholar
  72. Fozo EM, Scott-Anne K, Koo H, Quivey RG Jr (2007) Role of unsaturated fatty acid biosynthesis in virulence of Streptococcus mutans. Infect Immun 75:1537–1539Google Scholar
  73. Francis KP, Stewart GS (1997) Detection and speciation of bacteria through PCR using universal major cold-shock protein primer oligomers. J Ind Microbiol Biotechnol 19:286–293Google Scholar
  74. Frees D, Vogensen FK, Ingmer H (2003) Identification of proteins induced at low pH in Lactococcus lactis. Int J Food Microbiol 87:293–300Google Scholar
  75. Galhardo RS, Hastings PJ, Rosenberg SM (2007) Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol Biol 42:399–435Google Scholar
  76. Georgalaki MD, Sarantinopoulos P, Ferreira ES, De Vuyst L, Kalantzopoulos G, Tsakalidou E (2000) Biochemical properties of Streptococcus macedonicus strains isolated from Greek Kasseri cheese. J Appl Microbiol 88:817–825Google Scholar
  77. Georgalaki MD, Van Den Berghe E, Kritikos D, Devreese B, Van Beeumen J, Kalnatzpoulos G, De Vuyst L, Tsakalidou E (2002) Macedocin, a food-grade lantibiotic produced by Streptococcus macedonicus ACA-DC 198. Appl Environ Microbiol 68:5891–5903Google Scholar
  78. Gibson CM, Mallett TC, Claiborne A, Caparon MG (2000) Contribution of NADH oxidase to aerobic metabolism of Streptococcus pyogenes. J Bacteriol 182:448–455Google Scholar
  79. Giliberti G, Naclerio G, Martirani L, Ricca E, De Felice M (2002) Alteration of cell morphology and viability in a recA mutant of Streptococcus thermophilus upon induction of heat shock and nutrient starvation. Gene 295:1–6Google Scholar
  80. Giliberti G, Baccigalupi L, Cordone A, Ricca E, De Felice M (2006) Transcriptional analysis of the recA gene of Streptococcus thermophilus. Microb Cell Fact 5:29Google Scholar
  81. Glaser P, Rusniok C, Buchrieser C, Chevalier F, Frangeul L, Msadek T, Zouine M, Couve E, Lalioui L, Poyart C, Trieu-Cuot P, Kunst F (2002) Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol Microbiol 45:1499–1513Google Scholar
  82. Gong Y, Tian XL, Sutherlan T, Sisson G, Mai J, Ling J, Li YH (2009) Global transcriptional analysis of acid-inducible genes in Streptococcus mutans: multiple two-component systems involved in acid adaptation. Microbiology 155:3322–3332Google Scholar
  83. Gonzalez C, Hadany L, Ponder RG, Price M, Hastings PJ, Rosenberg SM (2008) Mutability and importance of a hypermutable cell subpopulation that produces stress-induced mutants in Escherichia coli. PLoS Genet 4:e1000208Google Scholar
  84. Gonzalez-Marquez H, Perrin C, Bracquart P, Guimont C, Linden G (1997) A 16 kDa protein family overexpressed by Streptococcus thermophilus PB18 in acid environments. Microbiology 143 (Pt 5):1587–1594Google Scholar
  85. Graca da Silveira M, Vitoria San Romao M, Loureiro-Dias MC, Rombouts FM, Abee T (2002) Flow cytometric assessment of membrane integrity of ethanol-stressed Oenococcus oeni cells. Appl Environ Microbiol 68:6087–6093Google Scholar
  86. Graham MR, Smoot LM, Migliaccio CA, Virtaneva K, Sturdevant DE, Porcella SF, Federle MJ, Adams GJ, Scott JR, Musser JM (2002) Virulence control in group A Streptococcus by a two-component gene regulatory system: global expression profiling and in vivo infection modeling. Proc Natl Acad Sci USA 99:13855–13860Google Scholar
  87. Graham MR, Virtaneva K, Porcella SF, Barry WT, Gowen BB, Johnson CR, Wright FA, Musser JM (2005) Group A Streptococcus transcriptome dynamics during growth in human blood reveals bacterial adaptive and survival strategies. Am J Pathol 166:455–465Google Scholar
  88. Graham MR, Virtaneva K, Porcella SF, Gardner DJ, Long RD, Welty DM, Barry WT, Johnson CA, Parkins LD, Wright FA, Musser JM (2006) Analysis of the transcriptome of group A Streptococcus in mouse soft tissue infection. Am J Pathol 169:927–942Google Scholar
  89. Griswold AR, Jameson-Lee M, Burne RA (2006) Regulation and physiologic significance of the agmatine deiminase system of Streptococcus mutans UA159. J Bacteriol 188:834–841Google Scholar
  90. Gryllos I, Grifantini R, Colaprico A, Cary ME, Hakansson A, Carey DW, Suarez-Chavez M, Kalish LA, Mitchell PD, White GL, Wessels MR (2008) PerR confers phagocytic killing resistance and allows pharyngeal colonization by group A Streptococcus. PLoS Pathog 4:e1000145Google Scholar
  91. Gunnewijk MG, Poolman B (2000) Phosphorylation state of HPr determines the level of expression and the extent of phosphorylation of the lactose transport protein of Streptococcus thermophilus. J Biol Chem 275:34073–34079Google Scholar
  92. Haas W, Kaushal D, Sublett J, Obert C, Tuomanen EI (2005) Vancomycin stress response in a sensitive and a tolerant strain of Streptococcus pneumoniae. J Bacteriol 187:8205–8210Google Scholar
  93. Hahn K, Faustoferri RC, Quivey RG Jr (1999) Induction of an AP endonuclease activity in Streptococcus mutans during growth at low pH. Mol Microbiol 31:1489–1498Google Scholar
  94. Hanks TS, Liu M, McClure MJ, Fukumura M, Duffy A, Lei B (2006) Differential regulation of iron- and manganese-specific MtsABC and heme-specific HtsABC transporters by the metalloregulator MtsR of group A Streptococcus. Infect Immun 74:5132–5139Google Scholar
  95. Hanna MN, Ferguson RJ, Li YH, Cvitkovitch DG (2001) uvrA is an acid-inducible gene involved in the adaptive response to low pH in Streptococcus mutans. J Bacteriol 183:5964–5973Google Scholar
  96. Hardie JM, Whiley RA (1997) Classification and overview of the genera Streptococcus and Enterococcus. Soc Appl Bacteriol Symp Ser 26:1S–11SGoogle Scholar
  97. Hartke A, Bouche S, Giard JC, Benachour A, Boutibonnes P, Auffray Y (1996) The lactic acid stress response of Lactococcus lactis subsp. lactis. Curr Microbiol 33:194–199Google Scholar
  98. Hasona A, Crowley PJ, Levesque CM, Mair RW, Cvitkovitch DG, Bleiweis AS, Brady LJ (2005) Streptococcal viability and diminished stress tolerance in mutants lacking the signal recognition particle pathway or YidC2. Proc Natl Acad Sci USA 102:17466–17471Google Scholar
  99. Hasona A, Zuobi-Hasona K, Crowley PJ, Abranches J, Ruelf MA, Bleiweis AS, Brady LJ (2007) Membrane composition changes and physiological adaptation by Streptococcus mutans signal recognition particle pathway mutants. J Bacteriol 189:1219–1230Google Scholar
  100. He X, Wu C, Yarbrough D, Sim L, Niu G, Merritt J, Shi W, Qi F (2008) The cia operon of Streptococcus mutans encodes a unique component required for calcium-mediated autoregulation. Mol Microbiol 70:112–126Google Scholar
  101. Hendriksen WT, Bootsma HJ, Estevao S, Hoogenboezem T, de Jong A, de Groot R, Kuipers OP, Hermans PW (2008) CodY of Streptococcus pneumoniae: link between nutritional gene regulation and colonization. J Bacteriol 190:590–601Google Scholar
  102. Higuchi M, Yamamoto Y, Poole LB, Shimada M, Sato Y, Takahashi N, Kamio Y (1999) Functions of two types of NADH oxidases in energy metabolism and oxidative stress of Streptococcus mutans. J Bacteriol 181:5940–5947Google Scholar
  103. Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N, Decaris B, Bolotin A, Delorme C, Dusko Ehrlich S, Guedon E, Monnet V, Renault P, Kleerebezem M (2005) New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol Rev 29:435–463Google Scholar
  104. Hussain H, Branny P, Allan E (2006) A eukaryotic-type serine/threonine protein kinase is required for biofilm formation, genetic competence, and acid resistance in Streptococcus mutans. J Bacteriol 188:1628–1632Google Scholar
  105. Ibrahim YM, Kerr AR, McCluskey J, Mitchell TJ (2004a) Control of virulence by the two-component system CiaR/H is mediated via HtrA, a major virulence factor of Streptococcus pneumoniae. J Bacteriol 186:5258–5266Google Scholar
  106. Ibrahim YM, Kerr AR, McCluskey J, Mitchell TJ (2004b) Role of HtrA in the virulence and competence of Streptococcus pneumoniae. Infect Immun 72:3584–3591Google Scholar
  107. Ibrahim YM, Kerr AR, Silva NA, Mitchell TJ (2005) Contribution of the ATP-dependent protease ClpCP to the autolysis and virulence of Streptococcus pneumoniae. Infect Immun 73:730–740Google Scholar
  108. Imlay JA, Linn S (1987) Mutagenesis and stress responses induced in Escherichia coli by hydrogen peroxide. J Bacteriol 169:2967–2976Google Scholar
  109. Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302–1309Google Scholar
  110. Imlay JA, Chin SM, Linn S (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240:640–642Google Scholar
  111. Janowiak BE, Griffith OW (2005) Glutathione synthesis in Streptococcus agalactiae. One protein accounts for gamma-glutamylcysteine synthetase and glutathione synthetase activities. J Biol Chem 280:11829–11839Google Scholar
  112. Jayaraman GC, Penders JE, Burne RA (1997) Transcriptional analysis of the Streptococcus mutans hrcA, grpE and dnaK genes and regulation of expression in response to heat shock and environmental acidification. Mol Microbiol 25:329–341Google Scholar
  113. Jiang SM, Cieslewicz MJ, Kasper DL, Wessels MR (2005) Regulation of virulence by a two-component system in group B Streptococcus. J Bacteriol 187:1105–1113Google Scholar
  114. Johri AK, Padilla J, Malin G, Paoletti LC (2003) Oxygen regulates invasiveness and virulence of group B Streptococcus. Infect Immun 71:6707–6711Google Scholar
  115. Kajfasz JK, Martinez AR, Rivera-Ramos I, Abranches J, Koo H, Quivey RG, Lemos JA (2009) Role of Clp proteins in expression of virulence properties of Streptococcus mutans. J Bacteriol 191:2060–2068Google Scholar
  116. Kajfasz JK, Rivera-Ramos I, Abranches J, Martinez AR, Rosalen PL, Derr AM, Quivey RG, Lemos JA (2010) Two Spx proteins modulate stress tolerance, survival, and virulence in Streptococcus mutans. J Bacteriol 192:2546–2556Google Scholar
  117. Kazmierczak KM, Wayne KJ, Rechtsteiner A, Winkler ME (2009) Roles of rel in stringent response, global regulation and virulence of serotype 2 Streptococcus pneumoniae D39. Mol Microbiol 72:590–611Google Scholar
  118. Keefe GP (1997) Streptococcus agalactiae mastitis: a review. Can Vet J 38:429–437Google Scholar
  119. Kim WS, Dunn NW (1997) Identification of a cold shock gene in lactic acid bacteria and the effect of cold shock on cryotolerance. Curr Microbiol 35:59–63Google Scholar
  120. Kim WS, Khunajakr N, Ren J, Dunn NW (1998) Conservation of the major cold shock protein in lactic acid bacteria. Curr Microbiol 37:333–336Google Scholar
  121. King KY, Horenstein JA, Caparon MG (2000) Aerotolerance and peroxide resistance in peroxidase and PerR mutants of Streptococcus pyogenes. J Bacteriol 182:5290–5299Google Scholar
  122. Kohler W (2007) The present state of species within the genera Streptococcus and Enterococcus. Int J Med Microbiol 297:133–150Google Scholar
  123. Krab IM, te Biesebeke R, Bernardi A, Parmeggiani A (2001) Elongation factor Ts can act as a steric chaperone by increasing the solubility of nucleotide binding-impaired elongation factor-Tu. Biochemistry 40:8531–8535Google Scholar
  124. Kreth J, Merritt J, Shi W, Qi F (2005) Co-ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species. Mol Microbiol 57:392–404Google Scholar
  125. Kreth J, Merritt J, Zhu L, Shi W, Qi F (2006) Cell density- and ComE-dependent expression of a group of mutacin and mutacin-like genes in Streptococcus mutans. FEMS Microbiol Lett 265:11–17Google Scholar
  126. Kreth J, Hung DC, Merritt J, Perry J, Zhu L, Goodman SD, Cvitkovitch DG, Shi W, Qi F (2007) The response regulator ComE in Streptococcus mutans functions both as a transcription activator of mutacin production and repressor of CSP biosynthesis. Microbiology 153:1799–1807Google Scholar
  127. Kwon HY, Kim SW, Choi MH, Ogunniyi AD, Paton JC, Park SH, Pyo SN, Rhee DK (2003) Effect of heat shock and mutations in ClpL and ClpP on virulence gene expression in Streptococcus pneumoniae. Infect Immun 71:3757–3765Google Scholar
  128. Kwon HY, Ogunniyi AD, Choi MH, Pyo SN, Rhee DK, Paton JC (2004) The ClpP protease of Streptococcus pneumoniae modulates virulence gene expression and protects against fatal pneumococcal challenge. Infect Immun 72:5646–5653Google Scholar
  129. Lamy MC, Zouine M, Fert J, Vergassola M, Couve E, Pellegrini E, Glaser P, Kunst F, Msadek T, Trieu-Cuot P, Poyart C (2004) CovS/CovR of group B Streptococcus: a two-component global regulatory system involved in virulence. Mol Microbiol 54:1250–1268Google Scholar
  130. Lancefield RC (1933) A serological differentiation of human and other groups of streptococci. J Exp Med 59:571–595Google Scholar
  131. Lemos JA, Burne RA (2002) Regulation and Physiological Significance of ClpC and ClpP in Streptococcus mutans. J Bacteriol 184:6357–6366Google Scholar
  132. Lemos JA, Burne RA (2008) A model of efficiency: stress tolerance by Streptococcus mutans. Microbiology 154:3247–3255Google Scholar
  133. Lemos JA, Chen YY, Burne RA (2001) Genetic and physiologic analysis of the groE operon and role of the HrcA repressor in stress gene regulation and acid tolerance in Streptococcus mutans. J Bacteriol 183:6074–6084Google Scholar
  134. Lemos JA, Brown TA Jr, Burne RA (2004) Effects of RelA on key virulence properties of planktonic and biofilm populations of Streptococcus mutans. Infect Immun 72:1431–1440Google Scholar
  135. Lemos JA, Abranches J, Burne RA (2005) Responses of cariogenic streptococci to environmental stresses. Curr Issues Mol Biol 7:95–107Google Scholar
  136. Lemos JA, Lin VK, Nascimento MM, Abranches J, Burne RA (2007a) Three gene products govern (p)ppGpp production by Streptococcus mutans. Mol Microbiol 65:1568–1581Google Scholar
  137. Lemos JA, Luzardo Y, Burne RA (2007b) Physiologic effects of forced down-regulation of dnaK and groEL expression in Streptococcus mutans. J Bacteriol 189:1582–1588Google Scholar
  138. Lemos JA, Nascimento MM, Lin VK, Abranches J, Burne RA (2008) Global regulation by (p)ppGpp and CodY in Streptococcus mutans. J Bacteriol 190:5291–5299Google Scholar
  139. Len AC, Harty DW, Jacques NA (2004a) Proteome analysis of Streptococcus mutans metabolic phenotype during acid tolerance. Microbiology 150:1353–1366Google Scholar
  140. Len AC, Harty DW, Jacques NA (2004b) Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance. Microbiology 150:1339–1351Google Scholar
  141. Levesque CM, Mair RW, Perry JA, Lau PC, Li YH, Cvitkovitch DG (2007) Systemic inactivation and phenotypic characterization of two-component systems in expression of Streptococcus mutans virulence properties. Lett Appl Microbiol 45:398–404Google Scholar
  142. Li LN, Guo LH, Lux R, Eckert R, Yarbrough D, He J, Anderson M, Shi WY (2010) Targeted antimicrobial therapy against Streptococcus mutans establishes protective non-cariogenic oral biofilms and reduces subsequent infection. Int J Oral Sci 2:66–73Google Scholar
  143. Li YH, Hanna MN, Svensater G, Ellen RP, Cvitkovitch DG (2001) Cell density modulates acid adaptation in Streptococcus mutans: implications for survival in biofilms. J Bacteriol 183:6875–6884Google Scholar
  144. Li YH, Lau PC, Tang N, Svensater G, Ellen RP, Cvitkovitch DG (2002a) Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans. J Bacteriol 184:6333–6342Google Scholar
  145. Li YH, Tang N, Aspiras MB, Lau PC, Lee JH, Ellen RP, Cvitkovitch DG (2002b) A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J Bacteriol 184:2699–2708Google Scholar
  146. Lin MY, Yen CL (1999) Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47:1460–1466Google Scholar
  147. Liu GY, Doran KS, Lawrence T, Turkson N, Puliti M, Tissi L, Nizet V (2004) Sword and shield: linked group B streptococcal beta-hemolysin/cytolysin and carotenoid pigment function to subvert host phagocyte defense. Proc Natl Acad Sci USA 101:14491–14496Google Scholar
  148. Lopez R, Gonzalez MP, Garcia E, Garcia JL, Garcia P (2000) Biological roles of two new murein hydrolases of Streptococcus pneumoniae representing examples of module shuffling. Res Microbiol 151:437–443Google Scholar
  149. Loughman JA, Caparon M (2006a) Regulation of SpeB in Streptococcus pyogenes by pH and NaCl: a model for in vivo gene expression. J Bacteriol 188:399–408Google Scholar
  150. Loughman JA, Caparon MG (2006b) A novel adaptation of aldolase regulates virulence in Streptococcus pyogenes. EMBO J 25:5414–5422Google Scholar
  151. Lu YJ, Rock CO (2006) Transcriptional regulation of fatty acid biosynthesis in Streptococcus pneumoniae. Mol Microbiol 59:551–566Google Scholar
  152. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, Shakhova V, Grigoriev I, Lou Y, Rohksar D, Lucas S, Huang K, Goodstein DM, Hawkins T, Plengvidhya V, Welker D, Hughes J, Goh Y, Benson A, Baldwin K, Lee JH, Diaz-Muniz I, Dosti B, Smeianov V, Wetcher W, Barabote R, Lorca G, Altermann E, Barrangou R, Ganesah B, Xie Y, Rawsthorne H, Tamir D, Parker C, Breidt F, Broadbent J, Hutkins R, O’Sullivan D, Steele J, Unlu G, Saier M, Klaenhammer T, Richardson P, Kozyavkin S, Weimer B, Mills D (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103:15611–15616Google Scholar
  153. Malke H, Ferretti JJ (2007) CodY-affected transcriptional gene expression of Streptococcus pyogenes during growth in human blood. J Med Microbiol 56:707–714Google Scholar
  154. Malke H, Steiner K, McShan WM, Ferretti JJ (2006) Linking the nutritional status of Streptococcus pyogenes to alteration of transcriptional gene expression: the action of CodY and RelA. Int J Med Microbiol 296:259–275Google Scholar
  155. Maragkoudakis PA, Papadelli M, Gerogalaki M, Panayotopoulos EG, Martinez-Gonzalez B, Mentis AF, Petraki K, Sgouras DN, Tsakalidou E (2009) In vitro and in vivo safety evaluation of the bacteriocin producer Streptococcus macedonicus ACA-DC 198. Int J Food Microbiol 133:141–147Google Scholar
  156. Marouni MJ, Sela S (2003) The luxS gene of Streptococcus pyogenes regulates expression of genes that affect internalization by epithelial cells. Infect Immun 71:5633–5639Google Scholar
  157. Marquis RE (1995) Oxygen metabolism, oxidative stress and acid-base physiology of dental plaque biofilms. J Ind Microbiol 15:198–207Google Scholar
  158. Marsh PD (2003) Are dental diseases examples of ecological catastrophes? Microbiology 149:279–294Google Scholar
  159. Martin-Galiano AJ, Overweg K, Ferrandiz MJ, Reuter M, Wells JM, de la Campa AG (2005) Transcriptional analysis of the acid tolerance response in Streptococcus pneumoniae. Microbiology 151:3935–3946Google Scholar
  160. Martinez AR, Abranches A, Kajfasz JK, Lemos JA (2010) Characterization of the Streptococcus sobrinus acid-stress response by interspecies microarrays and proteomics. Molec Oral Microbiol 25:331–342Google Scholar
  161. Martirani L, Raniello R, Naclerio G, Ricca E, De Felice M (2001) Identification of the DNA-binding protein, HrcA, of Streptococcus thermophilus. FEMS Microbiol Lett 198:177–182Google Scholar
  162. Mascher T, Heintz M, Zahner D, Merai M, Hakenbeck R (2006) The CiaRH system of Streptococcus pneumoniae prevents lysis during stress induced by treatment with cell wall inhibitors and by mutations in pbp2x involved in beta-lactam resistance. J Bacteriol 188:1959–1968Google Scholar
  163. McAllister LJ, Tseng HJ, Ogunniyi AD, Jennings MP, McEwan AG, Paton JC (2004) Molecular analysis of the psa permease complex of Streptococcus pneumoniae. Mol Microbiol 53:889–901Google Scholar
  164. Mereghetti L, Sitkiewicz I, Green NM, Musser JM (2008a) Extensive adaptive changes occur in the transcriptome of Streptococcus agalactiae (group B Streptococcus) in response to incubation with human blood. PLoS One 3:e3143Google Scholar
  165. Mereghetti L, Sitkiewicz I, Green NM, Musser JM (2008b) Remodeling of the Streptococcus agalactiae transcriptome in response to growth temperature. PLoS One 3:e2785Google Scholar
  166. Mereghetti L, Sitkiewicz I, Green NM, Musser JM (2009) Identification of an unusual pattern of global gene expression in group B Streptococcus grown in human blood. PLoS One 4:e7145Google Scholar
  167. Miyoshi A, Rochat T, Gratadoux JJ, Le Loir Y, Oliveira SC, Langella P, Azevedo V (2003) Oxidative stress in Lactococcus lactis. Genet Mol Res 2:348–359Google Scholar
  168. Nair S, Poyart C, Beretti JL, Veiga-Fernandes H, Berche P, Trieu-Cuot P (2003) Role of the Streptococcus agalactiae ClpP serine protease in heat-induced stress defence and growth arrest. Microbiology 149:407–417Google Scholar
  169. Nakayama K (1992) Nucleotide sequence of Streptococcus mutans superoxide dismutase gene and isolation of insertion mutants. J Bacteriol 174:4928–4934Google Scholar
  170. Nascimento MM, Lemos JA, Abranches J, Goncalves RB, Burne RA (2004) Adaptive acid tolerance response of Streptococcus sobrinus. J Bacteriol 186:6383–6390Google Scholar
  171. Nascimento MM, Lemos JA, Abranches J, Lin VK, Burne RA (2008) Role of RelA of Streptococcus mutans in global control of gene expression. J Bacteriol 190:28–36Google Scholar
  172. Naumann D, Helm D, Labischinski H (1991) Microbiological characterizations by FT-IR spectroscopy. Nature 351:81–82Google Scholar
  173. Neuhaus FC, Baddiley J (2003) A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in Gram-positive bacteria. Microbiol Mol Biol Rev 67:686–723Google Scholar
  174. Nguyen PT, Abranches J, Phan TN, Marquis RE (2002) Repressed respiration of oral streptococci grown in biofilms. Curr Microbiol 44:262–266Google Scholar
  175. Nicodeme M, Perrin C, Hols P, Bracquart P, Gaillard JL (2004) Identification of an iron-binding protein of the Dps family expressed by Streptococcus thermophilus. Curr Microbiol 48:51–56Google Scholar
  176. Niven GW, Mulholland F (1998) Cell membrane integrity and lysis in Lactococcus lactis: the detection of a population of permeable cells in post-logarithmic phase cultures. J Appl Microbiol 84:90–96Google Scholar
  177. Novakova L, Saskova L, Pallova P, Janececk J, Novotna J, Ulrych A, Echenique J, Trombe MC, Branny P (2005) Characterization of a eukaryotic type serine/threonine protein kinase and protein phosphatase of Streptococcus pneumoniae and identification of kinase substrates. FEBS J 272:1243–1254Google Scholar
  178. O’Driscoll B, Gahan CG, Hill C (1996) Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence. Appl Environ Microbiol 62:1693–1698Google Scholar
  179. Ogier JC, Serror P (2008) Safety assessment of dairy microorganisms: the Enterococcus genus. Int J Food Microbiol 126:291–301Google Scholar
  180. Olsen RJ, Sitkiewicz I, Ayeras AA, Gonulal VE, Cantu C, Beres SB, Green NM, Lei B, Humbird T, Greaver J, Chang E, Ragasa WP, Montgomery CA, Cartwright J, McGeer A, Low DE, Whitney AR, Cagle PT, Blasdel TL, DeLeo FR, Musser JM (2010) Decreased necrotizing fasciitis capacity caused by a single nucleotide mutation that alters a multiple gene virulence axis. Proc Natl Acad Sci USA 107:888–893Google Scholar
  181. O’Sullivan E, Condon S (1999) Relationship between acid tolerance, cytoplasmic pH, and ATP and H+-ATPase levels in chemostat cultures of Lactococcus lactis. Appl Environ Microbiol 65:2287–2293Google Scholar
  182. Panoff J-M, Thammavongs B, Laplace J-M, Hartke A, Boutibonnes P, Auffray Y (1995) Cryotolerance and cold adaptation in Lactococcus lactis subsp. lactis IL1403. Cryobiology 32:516–520Google Scholar
  183. Papadimitriou K, Pratsinis H, Nebe-von-Caron G, Kletsas D, Tsakalidou E (2006) Rapid assessment of the physiological status of Streptococcus macedonicus by flow cytometry and fluorescence probes. Int J Food Microbiol 111:197–205Google Scholar
  184. Papadimitriou K, Pratsinis H, Nebe-von-Caron G, Kletsas D, Tsakalidou E (2007) Acid tolerance of Streptococcus macedonicus as assessed by flow cytometry and single-cell sorting. Appl Environ Microbiol 73:465–476Google Scholar
  185. Papadimitriou K, Boutou E, Zoumpopoulos G, Tarantilis PA, Polissiou M, Vorgias CE, Tsakalidou E (2008) RNA arbitrarily primed PCR and Fourier transform infrared spectroscopy reveal plasticity in the acid tolerance response of Streptococcus macedonicus. Appl Environ Microbiol 74:6068–6076Google Scholar
  186. Park CY, Kim EH, Choi SW, Tran TD, Kim IH, Kim SN, Pyo S, Rhee DK (2010) Virulence attenuation of Streptococcus pneumoniae clpP mutant by sensitivity to oxidative stress in macrophages via an NO-mediated pathway. J Microbiol 48:229–235Google Scholar
  187. Paterson GK, Blue CE, Mitchell TJ (2006) An operon in Streptococcus pneumoniae containing a putative alkylhydroperoxidase D homologue contributes to virulence and the response to oxidative stress. Microb Pathog 40:152–160Google Scholar
  188. Pebay M, Holl AC, Simonet JM, Decaris B (1995) Characterization of the gor gene of the lactic acid bacterium Streptococcus thermophilus CNRZ368. Res Microbiol 146:371–383Google Scholar
  189. Pericone CD, Park S, Imlay JA, Weiser JN (2003) Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the Fenton reaction. J Bacteriol 185:6815–6825Google Scholar
  190. Perrin C, Guimont C, Bracquart P, Gaillard JL (1999) Expression of a new cold shock protein of 21.5 kDa and of the major cold shock protein by Streptococcus thermophilus after cold shock. Curr Microbiol 39:342–347Google Scholar
  191. Petersen FC, Tao L, Scheie AA (2005) DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation. J Bacteriol 187:4392–4400Google Scholar
  192. Phares CR, Lynfield R, Farley MM, Mohle-Boetani J, Harrison LH, Petit S, Craig AS, Schaffner W, Zansky SM, Gershman K, Stefonek KR, Albanese BA, Zell ER, Schuchat A, Schrag SJ (2008) Epidemiology of invasive group B streptococcal disease in the United States, 1999–2005. JAMA 299:2056–2065Google Scholar
  193. Poirazi P, Leroy F, Georgalaki MD, Aktypis A, De Vuyst L, Tsakalidou E (2007) Use of artificial neural networks and a gamma-concept-based approach to model growth of and bacteriocin production by Streptococcus macedonicus ACA-DC 198 under simulated conditions of Kasseri cheese production. Appl Environ Microbiol 73:768–776Google Scholar
  194. Potrykus K, Cashel M (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62:35–51Google Scholar
  195. Poyart C, Pellegrini E, Gaillot O, Boumaila C, Baptista M, Trieu-Cuot P (2001) Contribution of Mn-cofactored superoxide dismutase (SodA) to the virulence of Streptococcus agalactiae. Infect Immun 69:5098–5106Google Scholar
  196. Qi F, Merritt J, Lux R, Shi W (2004) Inactivation of the ciaH gene in Streptococcus mutans diminishes mutacin production and competence development, alters sucrose-dependent biofilm formation, and reduces stress tolerance. Infect Immun 72:4895–4899Google Scholar
  197. Quach D, van Sorge NM, Kristian SA, Bryan JD, Shelver DW, Doran KS (2009) The CiaR response regulator in group B Streptococcus promotes intracellular survival and resistance to innate immune defenses. J Bacteriol 191:2023–2032Google Scholar
  198. Quivey RG Jr, Faustoferri R, Monahan K, Marquis R (2000) Shifts in membrane fatty acid profiles associated with acid adaptation of Streptococcus mutans. FEMS Microbiol Lett 189:89–92Google Scholar
  199. Quivey RG, Kuhnert WL, Hahn K (2001) Genetics of acid adaptation in oral streptococci. Crit Rev Oral Biol Med 12:301–314Google Scholar
  200. Rallu F, Gruss A, Maguin E (1996) Lactococcus lactis and stress. Antonie van Leeuwenhoek 70:243–251Google Scholar
  201. Rallu F, Gruss A, Ehrlich SD, Maguin E (2000) Acid- and multistress-resistant mutants of Lactococcus lactis: identification of intracellular stress signals. Mol Microbiol 35:517–528Google Scholar
  202. Rathsam C, Eaton RE, Simpson CL, Browne GV, Berg T, Harty DW, Jacques NA (2005) Up-regulation of competence- but not stress-responsive proteins accompanies an altered metabolic phenotype in Streptococcus mutans biofilms. Microbiology 151:1823–1837Google Scholar
  203. Renye JA Jr, Piggot PJ, Daneo-Moore L, Buttaro BA (2004) Persistence of Streptococcus mutans in stationary-phase batch cultures and biofilms. Appl Environ Microbiol 70:6181–6187Google Scholar
  204. Ricci S, Janulczyk R, Bjorck L (2002) The regulator PerR is involved in oxidative stress response and iron homeostasis and is necessary for full virulence of Streptococcus pyogenes. Infect Immun 70:4968–4976Google Scholar
  205. Robertson GT, Ng WL, Foley J, Gilmour R, Winkler ME (2002) Global transcriptional analysis of clpP mutations of type 2 Streptococcus pneumoniae and their effects on physiology and virulence. J Bacteriol 184:3508–3520Google Scholar
  206. Robertson GT, Ng WL, Gilmour R, Winkler ME (2003) Essentiality of clpX, but not clpP, clpL, clpC, or clpE, in Streptococcus pneumoniae R6. J Bacteriol 185:2961–2966Google Scholar
  207. Rolerson E, Swick A, Newlon L, Palmer C, Pan Y, Keeshan B, Spatafora G (2006) The SloR/Dlg metalloregulator modulates Streptococcus mutans virulence gene expression. J Bacteriol 188:5033–5044Google Scholar
  208. Rosenbach FJ (1884) Mikro-organismen bei den Wund-Infections-Krankheiten des Menschen [in German]. WeisbadenGoogle Scholar
  209. Ryan CS, Kleinberg I (1995) Bacteria in human mouths involved in the production and utilization of hydrogen peroxide. Arch Oral Biol 40:753–763Google Scholar
  210. Santi I, Grifantini R, Jiang SM, Brettoni C, Grandi G, Wessels MR, Soriani M (2009) CsrRS regulates group B Streptococcus virulence gene expression in response to environmental pH: a new perspective on vaccine development. J Bacteriol 191:5387–5397Google Scholar
  211. Saskova L, Novakova L, Basler M, Branny P (2007) Eukaryotic-type serine/threonine protein kinase StkP is a global regulator of gene expression in Streptococcus pneumoniae. J Bacteriol 189:4168–4179Google Scholar
  212. Savijoki K, Ingmer H, Frees D, Vogensen FK, Palva A, Varmanen P (2003) Heat and DNA damage induction of the LexA-like regulator HdiR from Lactococcus lactis is mediated by RecA and ClpP. Mol Microbiol 50:609–621Google Scholar
  213. Schlegel L, Grimont F, Ageron E, Grimont PA, Bouvet A (2003) Reappraisal of the taxonomy of the Streptococcus bovis/Streptococcus equinus complex and related species: description of Streptococcus gallolyticus subsp. gallolyticus subsp. nov., S. gallolyticus subsp. macedonicus subsp. nov. and S. gallolyticus subsp. pasteurianus subsp. nov. Int J Syst Evol Microbiol 53:631–645Google Scholar
  214. Schleifer KH, Kilpper-Balz R (1984) Transfer of Streptococcus faecalis and Streptococcus faecium to the genus Enterococcus nom. rev. as Enterococcus faecalis comb. nov. and Enterococcus faecium comb. nov. Int J Syst Bacteriol 34:31–34Google Scholar
  215. Schleifer KH, Kraus J, Dvorak C (1985) Transfer of Streptococcus lactis and related Streptococci to the genus lactococcus gen. nov. Syst Appl Microbiol 6:183–195Google Scholar
  216. Senadheera D, Krastel K, Mair R, Persadmehr A, Abranches J, Burne RA, Cvitkovitch DG (2009) Inactivation of VicK affects acid production and acid survival of Streptococcus mutans. J Bacteriol 191:6415–6424Google Scholar
  217. Shelburne SA, III, Sumby P, Sitkiewicz I, Granville C, DeLeo FR, Musser JM (2005) Central role of a bacterial two-component gene regulatory system of previously unknown function in pathogen persistence in human saliva. Proc Natl Acad Sci USA 102:16037–16042Google Scholar
  218. Shelburne SA, III, Keith D, Horstmann N, Sumby P, Davenport MT, Graviss EA, Brennan RG, Musser JM (2008a) A direct link between carbohydrate utilization and virulence in the major human pathogen group A Streptococcus. Proc Natl Acad Sci USA 105:1698–1703Google Scholar
  219. Shelburne SA, Davenport MT, Keith DB, Musser JM (2008b) The role of complex carbohydrate catabolism in the pathogenesis of invasive streptococci. Trends Microbiol 16:318–325Google Scholar
  220. Sheng J, Marquis RE (2006) Enhanced acid resistance of oral streptococci at lethal pH values associated with acid-tolerant catabolism and with ATP synthase activity. FEMS Microbiol Lett 262:93–98Google Scholar
  221. Sheng J, Marquis RE (2007) Malolactic fermentation by Streptococcus mutans. FEMS Microbiol Lett 272:196–201Google Scholar
  222. Sherman JM (1937) The streptococci. Bacteriol Rev 1:3–97Google Scholar
  223. Sherman JM, Albus WR (1918) Some characters which differentiate the lactic-acid Streptococcus from streptococci of the pyogenes type occurring in milk. J Bacteriol 3:153–174Google Scholar
  224. Sherrill C, Fahey RC (1998) Import and metabolism of glutathione by Streptococcus mutans. J Bacteriol 180:1454–1459Google Scholar
  225. Shet A, Ferrieri P (2004) Neonatal & maternal group B streptococcal infections: a comprehensive review. Ind J Med Res 120:141–150Google Scholar
  226. Shottmuller H (1903) Die Artunterscheidung der fur den menschen Pathogen Streptokokken durch Blutagar [in German]. Munch Med Wochenschr 50:849–853Google Scholar
  227. Siller M, Janapatla RP, Pirzada ZA, Hassler C, Zinkl D, Charpentier E (2008) Functional analysis of the group A streptococcal luxS/AI-2 system in metabolism, adaptation to stress and interaction with host cells. BMC Microbiol 8:188Google Scholar
  228. Simmen HP, Blaser J (1993) Analysis of pH and pO2 in abscesses, peritoneal fluid, and drainage fluid in the presence or absence of bacterial infection during and after abdominal surgery. Am J Surg 166:24–27Google Scholar
  229. Sitkiewicz I, Musser JM (2009) Analysis of growth-phase regulated genes in Streptococcus agalactiae by global transcript profiling. BMC Microbiol 9:32Google Scholar
  230. Sitkiewicz I, Green NM, Guo N, Bongiovanni AM, Witkin SS, Musser JM (2009) Transcriptome adaptation of group B Streptococcus to growth in human amniotic fluid. PLoS One 4:e6114Google Scholar
  231. Smart JB, Thomas TD (1987) Effect of oxygen on lactose metabolism in lactic streptococci. Appl Environ Microbiol 53:533–541Google Scholar
  232. Smoot LM, Smoot JC, Graham MR, Somerville GA, Sturdevant DE, Migliaccio CA, Sylva GL, Musser JM (2001) Global differential gene expression in response to growth temperature alteration in group A Streptococcus. Proc Natl Acad Sci USA 98:10416–10421Google Scholar
  233. Sonenshein AL (2005) CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr Opin Microbiol 8:203–207Google Scholar
  234. Sturr MG, Marquis RE (1992) Comparative acid tolerances and inhibitor sensitivities of isolated F-ATPases of oral lactic acid bacteria. Appl Environ Microbiol 58:2287–2291Google Scholar
  235. Centers for Disease Control and Prevention (2001) Promoting oral health: interventions for preventing dental caries, oral and pharyngeal cancers, and sports-related craniofacial injuries. MMWR Recomm Rep 50(RR21):1–13Google Scholar
  236. Teraguchi S, Ono J, Kiyosawa I, Okonogi S (1987) Oxygen uptake activity and aerobic metabolism of Streptococcus thermophilus STH450. J Dairy Sci 70:514–523Google Scholar
  237. Tettelin H, Nelson KE, Paulsen IT, Elsen JA, Read TD, Peterson S, Heidelberg J, DeBoy RT, Haft DH, Dodson RJ, Durkin AS, Gwinn M, Kolonay JF, Nelson WC, Peterson JD, Umayam LA, White O, Salzberg SL, Lewis MR, Radune D, Holtzapple E, Khouri H, Wolf AM, Utterback TR, Hansen CL, McDonald LA, Feldblyum TV, Angiuoli S, Dickinson T, Hickey EK, Holt IE, Loftus BJ, Yang F, Smith HO, Venter JC, Dougherty BA, Morrison DA, Holingshead SK, Fraser CM (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293:498–506Google Scholar
  238. Tettelin H., Masignani V, Cieslewicz MJ, Eisen JA, Peterson S, Wessels MR, Paulsen I, Nelson KE, Margarit I, Read TD, Madoff LC, Wolf AM, Beanan MJ, Brinkac LM, Daugherty SC, DeBoy RT, Durkin AS, Kolonay JF, Madupu R, Lewis MR, Radune D, Fedorova NB, Scanlan D, Khouri H, Mulligan S, Carty HA, Cline RT, Van Aken SE, Gill J, Scarselli M, Mora M, Iacobini ET, Brettoni C, Galli G, Mariani M, Vegni F, Maione D, Rinaudo D, Rappuoli R, Telford JL, Kasper DL, Grandi G, Fraser CM (2002) Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proc Natl Acad Sci USA 99:12391–12396Google Scholar
  239. Tettelin H, Msignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, Deboy RT, Davidsen TM, Mora M, Scarselli M, Margarit Ros I, Peterson JD, Hauser CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou L, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K, O’Connor KJ, Smith S, Utterback TR, White O, Rubens CE, Grandi G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser CM (2005) Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome.” Proc Natl Acad Sci USA 102:13950–13955Google Scholar
  240. Thibessard A, Fernandez A, Gintz B, Leblond-Bourget N, Decaris B (2001a) Hydrogen peroxide effects on Streptococcus thermophilus CNRZ368 cell viability. Res Microbiol 152:593–596Google Scholar
  241. Thibessard A, Leblond-Bourget N, Fernandez A, Gintz B, Decaris B (2001b) Response of Streptococcus thermophilus CNRZ368 and its colonial variants to oxidative stress: evidence for an inducible defence system. Lait 81:311–316Google Scholar
  242. Thibessard A, Fernandez A, Gintz B, Leblond-Bourget N, Decaris B (2002) Effects of rodA and pbp2b disruption on cell morphology and oxidative stress response of Streptococcus thermophilus CNRZ368. J Bacteriol 184:2821–2826Google Scholar
  243. Thibessard A, Borges F, Fernandez A, Gintz B, Decaris B, Leblond-Bourget N (2004) Identification of Streptococcus thermophilus CNRZ368 genes involved in defense against superoxide stress. Appl Environ Microbiol 70:2220–2229Google Scholar
  244. Throup JP, Koretke KK, Bryant AP, Ingraham KA, Chalker AF, Ge Y, Marra A, Wallis NG, Brown JR, Holmes DJ, Rosenberg M, Burnham MK (2000) A genomic analysis of two-component signal transduction in Streptococcus pneumoniae. Mol Microbiol 35:566–576Google Scholar
  245. Tong H, Chen W, Merritt J, Qi F, Shi W, Dong X (2007) Streptococcus oligofermentans inhibits Streptococcus mutans through conversion of lactic acid into inhibitory H2O2: a possible counteroffensive strategy for interspecies competition. Mol Microbiol 63:872–880Google Scholar
  246. Tsakalidou E, Zoidou E, Pot B, Wassill L, Ludwig W, Devriese LA, Kalantzopoulos G, Schleifer KH, Kersters K (1998) Identification of streptococci from Greek Kasseri cheese and description of Streptococcus macedonicus sp. nov. Int J Syst Bacteriol 48 (Pt 2):519–527Google Scholar
  247. Tseng HJ, McEwan AG, Paton JC, Jennings MP (2002) Virulence of Streptococcus pneumoniae: PsaA mutants are hypersensitive to oxidative stress. Infect Immun 70:1635–1639Google Scholar
  248. Tsou CC, Chiang-Ni C, Lin YS, Chuang WJ, Lin MT, Liu CC, Wu JJ (2008) An iron-binding protein, Dpr, decreases hydrogen peroxide stress and protects Streptococcus pyogenes against multiple stresses. Infect Immun 76:4038–4045Google Scholar
  249. Tu le N, Jeong HY, Kwon HY, Ogunniyi AD, Paton JC, Pyo SN, Rhee DK (2007) Modulation of adherence, invasion, and tumor necrosis factor alpha secretion during the early stages of infection by Streptococcus pneumoniae ClpL. Infect Immun 75:2996–3005Google Scholar
  250. Turlan C, Prudhomme M, Fichant G, Martin B, Gutierrez C (2009) SpxA1, a novel transcriptional regulator involved in X-state (competence) development in Streptococcus pneumoniae. Mol Microbiol 73:492–506Google Scholar
  251. Urban CF, Lourido S, Zychlinsky A (2006) How do microbes evade neutrophil killing? Cell Microbiol 8:1687–1696Google Scholar
  252. Vaillancourt K, Moineau S, Frenette M, Lessard C, Vadeboncoeur C (2002) Galactose and lactose genes from the galactose-positive bacterium Streptococcus salivarius and the phylogenetically related galactose-negative bacterium Streptococcus thermophilus: organization, sequence, transcription, and activity of the gal gene products. J Bacteriol 184:785–793Google Scholar
  253. van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E (2002) Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek 82:187–216Google Scholar
  254. Van den Berghe E, Skourtas G, Tsakalidou E, De Vuyst L (2006) Streptococcus macedonicus ACA-DC 198 produces the lantibiotic, macedocin, at temperature and pH conditions that prevail during cheese manufacture. Int J Food Microbiol 107:138–147Google Scholar
  255. van den Bogaard PT, Kleerebezem M, Kuipers OP, de Vos WM (2000) Control of lactose transport, beta-galactosidase activity, and glycolysis by CcpA in Streptococcus thermophilus: evidence for carbon catabolite repression by a non-phosphoenolpyruvate-dependent phosphotransferase system sugar. J Bacteriol 182:5982–5989Google Scholar
  256. Varcamonti M, Graziano MR, Pezzopane R, Naclerio G, Arsenijevic S, De Felice M (2003) Impaired temperature stress response of a Streptococcus thermophilus deoD mutant. Appl Environ Microbiol 69:1287–1289Google Scholar
  257. Varcamonti M, Arsenijevic S, Martirani L, Fusco D, Naclerio G, De Felice M (2006) Expression of the heat shock gene clpL of Streptococcus thermophilus is induced by both heat and cold shock. Microb Cell Fact 5:6Google Scholar
  258. Virtaneva K, Graham MR, Porcella SF, Hoe NP, Su H, Graviss EA, Gardner TJ, Allison JE, Lemon WJ, Bailey JR, Parnell MJ, Musser JM (2003) Group A Streptococcus gene expression in humans and cynomolgus macaques with acute pharyngitis. Infect Immun 71:2199–2207Google Scholar
  259. Virtaneva K, Porcella SF, Graham MR, Ireland RM, Johnson CA, Ricklefs SM, Babar I, Parkins LD, Romero RA, Corn GJ, Gardner DJ, Bailey JR, Parnell MJ, Musser JM (2005) Longitudinal analysis of the group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc Natl Acad Sci USA 102:9014–9019Google Scholar
  260. Voyich JM, Braughton KR, Sturdevant DE, Vuong C, Kobayashi SD, Porcella SD, Otto M, Musser JM, DeLeo FR (2004a) Engagement of the pathogen survival response used by group A Streptococcus to avert destruction by innate host defense. J Immunol 173:1194–1201Google Scholar
  261. Voyich JM, Musser JM, DeLeo FR (2004b) Streptococcus pyogenes and human neutrophils: a paradigm for evasion of innate host defense by bacterial pathogens. Microbes Infect 6:1117–1123Google Scholar
  262. Welin J, Wilkins JC, Beighton D, Wrzesinski K, Fey SJ, Mose-Larsen P, Hamilton IR, Svensater G (2003) Effect of acid shock on protein expression by biofilm cells of Streptococcus mutans. FEMS Microbiol Lett 227:287–293Google Scholar
  263. Wen ZT, Burne RA (2004) LuxS-mediated signaling in Streptococcus mutans is involved in regulation of acid and oxidative stress tolerance and biofilm formation. J Bacteriol 186:2682–2691Google Scholar
  264. Wen ZT, Suntharaligham P, Cvitkovitch DG, Burne RA (2005) Trigger factor in Streptococcus mutans is involved in stress tolerance, competence development, and biofilm formation. Infect Immun 73:219–225Google Scholar
  265. Wen ZT, Baker HV, Burne RA (2006) Influence of BrpA on critical virulence attributes of Streptococcus mutans. J Bacteriol 188:2983–2992Google Scholar
  266. WHO (2007) Pneumococcal conjugate vaccine for childhood immunization – World Health Organization position paper. Wkly Epidemiol Rec 82:93–104Google Scholar
  267. Wilkins JC, Homer KA, Beighton D (2002) Analysis of Streptococcus mutans proteins modulated by culture under acidic conditions. Appl Environ Microbiol 68:2382–2390Google Scholar
  268. Witte G, Hartung S, Buttner K, Hopfner KP (2008) Structural biochemistry of a bacterial checkpoint protein reveals diadenylate cyclase activity regulated by DNA recombination intermediates. Mol Cell 30:167–178Google Scholar
  269. Wouters JA, Sanders JW, Kok J, de Vos WM, Kuipers OP, Abee T (1998) Clustered organization and transcriptional analysis of a family of five csp genes of Lactococcus lactis MG1363. Microbiology 144 (Pt 10):2885–2893Google Scholar
  270. Wouters JA, Rombouts FM, de Vos WM, Kuipers OP, Abee T (1999) Cold shock proteins and low-temperature response of Streptococcus thermophilus CNRZ302. Appl Environ Microbiol 65:4436–4442Google Scholar
  271. Yamamoto Y, Higuchi M, Poole LB, Kamio Y (2000) Role of the dpr product in oxygen tolerance in Streptococcus mutans. J Bacteriol 182:3740–3747Google Scholar
  272. Yamamoto Y, Poyart C, Trieu-Cuot P, Lamberet G, Gruss A, Gaudu P (2005) Respiration metabolism of group B Streptococcus is activated by environmental haem and quinone and contributes to virulence. Mol Microbiol 56:525–534Google Scholar
  273. Yamamoto Y, Pargade V, Lamberet G, Gaudu P, Thomas F, Texereau J, Gruss A, Trieu-Cuot P, Poyart C (2006) The group B Streptococcus NADH oxidase Nox-2 is involved in fatty acid biosynthesis during aerobic growth and contributes to virulence. Mol Microbiol 62:772–785Google Scholar
  274. Yamashita Y, Takehara T, Kuramitsu HK (1993) Molecular characterization of a Streptococcus mutans mutant altered in environmental stress responses. J Bacteriol 175:6220–6228Google Scholar
  275. Yesilkaya H, Kadioglu A, Gingles N, Alexander JE, Mitchell TJ, Andrew PW (2000) Role of manganese-containing superoxide dismutase in oxidative stress and virulence of Streptococcus pneumoniae. Infect Immun 68:2819–2826Google Scholar
  276. Yu J, Bryant AP, Marra A, Lonetto MA, Ingraham KA, Chalker AF, Holmes DJ, Holden D, Rosenberg M, McDevitt D (2001) Characterization of the Streptococcus pneumoniae NADH oxidase that is required for infection. Microbiology 147:431–438Google Scholar
  277. Zhang J, Biswas I (2009) 3′-Phosphoadenosine-5′-phosphate phosphatase activity is required for superoxide stress tolerance in Streptococcus mutans. J Bacteriol 191:4330–4340Google Scholar
  278. Zhang Q, Xu SX, Wang H, Xu WC, Zhang XM, Wu KF, Liu L, Yin YB (2009) Contribution of ClpE to virulence of Streptococcus pneumoniae. Can J Microbiol 55:1187–1194Google Scholar
  279. Zhu L, Kreth J (2010) Role of Streptococcus mutans eukaryotic-type serine/threonine protein kinase in interspecies interactions with Streptococcus sanguinis. Arch Oral Biol 55:385–390Google Scholar
  280. Zotta T, Asterinou K, Rossano R, Ricciardi A, Varcamonti M, Parente E (2009) Effect of inactivation of stress response regulators on the growth and survival of Streptococcus thermophilus Sfi39. Int J Food Microbiol 129:211–220Google Scholar
  281. Zoumpopoulou G, Foligne B, Christodoulou K, Grangette C, Pot B, Tsakalidou E (2008) Lactobacillus fermentum ACA-DC 179 displays probiotic potential in vitro and protects against trinitrobenzene sulfonic acid (TNBS)-induced colitis and Salmonella infection in murine models. Int J Food Microbiol 121:18–26Google Scholar
  282. Zuber P (2004) Spx-RNA polymerase interaction and global transcriptional control during oxidative stress. J Bacteriol 186:1911–1918Google Scholar

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© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Center for Oral Biology and Department of Microbiology and ImmunologyUniversity of Rochester Medical CenterRochesterUSA
  2. 2.Laboratory of Dairy Research, Department of Food Science and TechnologyAgricultural University of AthensAthensGreece

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