Responses of Lactic Acid Bacteria to Acid Stress

  • Jessica K. Kajfasz
  • Robert G. QuiveyJr.
Part of the Food Microbiology and Food Safety book series (FMFS)


Lactic acid bacteria (LAB) are a diverse group of Gram-positive microbes that ferment carbohydrates to organic acids, primarily lactic acid. LAB include organisms vitally important to the production of foods, bread, and wine, and they include major human pathogens for diseases of the oropharyneal space, lungs, mouth, and skin. For all of these organs, the production of lactic acid rapidly and substantially lowers the pH of their external environments. Because bacterial membranes are essentially porous to protons, these bacteria are at risk of damaging cellular constituents to the extent that growth ceases, and eventually they do not survive. Thus, the LAB have evolved a broad range of mechanisms to protect themselves from acidification, to repair cellular damage, and to use low-pH environments to outcompete other bacteria. In this chapter, we describe the acid-stress-responsive mechanisms of representative LAB, which have provided a framework of how these organisms respond to, and prosper in, acidic environments.


Lactic Acid Bacterium Acid Resistance Acid Stress Acid Tolerance Proton Motive Force 
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. Aas JA, Griffen AL, Dardis SR, Lee AM, Olsen I, Dewhirst FE, Leys EJ, Paster BJ (2008) Bacteria of dental caries in primary and permanent teeth in children and young adults. J Clin Microbiol 46:1407–1417CrossRefGoogle Scholar
  2. Ajdic D, McShan 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 99:14434–14439CrossRefGoogle Scholar
  3. Ansanay V, Dequin S, Blondin B, Barre P (1993) Cloning, sequence and expression of the gene encoding the malolactic enzyme from Lactococcus lactis. FEBS Lett 332:74–80CrossRefGoogle Scholar
  4. Araque I, Gil J, Carrete R, Bordons A, Reguant C (2009) Detection of arc genes related with the ethyl carbamate precursors in wine lactic acid bacteria. J Agric Food Chem 57:1841–1847CrossRefGoogle Scholar
  5. Arena ME, Manca de Nadra MC, Munoz R (2002) The arginine deiminase pathway in the wine lactic acid bacterium Lactobacillus hilgardii X1B: structural and functional study of the arcABC genes. Gene 301:61–66CrossRefGoogle Scholar
  6. Azcarate-Peril MA, Altermann E, Hoover-Fitzula RL, Cano RJ, Klaenhammer TR (2004) Identification and inactivation of genetic loci involved with Lactobacillus acidophilus acid tolerance. Appl Environ Microbiol 70:5315–5322CrossRefGoogle Scholar
  7. Bandell M, Ansanay V, Rachidi N, Dequin S, Lolkema JS (1997) Membrane potential-generating malate (MleP) and citrate (CitP) transporters of lactic acid bacteria are homologous proteins. Substrate specificity of the 2-hydroxycarboxylate transporter family. J Biol Chem 272:18140–18146CrossRefGoogle Scholar
  8. Becker MR, Paster BJ, Leys EJ, Moeschberger ML, Kenyon SG, Galvin JL, Boches SK, Dewhirst FE, Griffen AL (2002) Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol 40:1001–1009CrossRefGoogle Scholar
  9. Beier BD, Quivey RGJ, Berger AJ (2010) Identification of different bacterial species in biofilms using confocal raman microscopy. J Biomed Opt 15(6):066001CrossRefGoogle Scholar
  10. Belli WA, Marquis RE (1991) Adaptation of Streptococcus mutans and Enterococcus hirae to acid stress in continuous culture. Appl Environ Microbiol 57:1134–1138Google Scholar
  11. Belli WA, Marquis RE (1994) Catabolite modification of acid tolerance of Streptococcus mutans GS-5. Oral Microbiol Immunol 9:29–34CrossRefGoogle Scholar
  12. Belli WA, Buckley DH, Marquis RE (1995) Weak acid effects and fluoride inhibition of glycolysis by Streptococcus mutans GS-5. Can J Microbiol 41:785–791CrossRefGoogle Scholar
  13. Beltramo C, Grandvalet C, Pierre F, Guzzo J (2004) Evidence for multiple levels of regulation of Oenococcus oeni clpP-clpL locus expression in response to stress. J Bacteriol 186:2200–2205CrossRefGoogle Scholar
  14. Bender GR, Sutton SV, Marquis RE (1986) Acid tolerance, proton permeabilities, and membrane ATPases of oral streptococci. Infect Immun 53:331–338Google Scholar
  15. Bender GR, Marquis RE (1987) Membrane ATPases and acid tolerance of Actinomyces viscosus and Lactobacillus casei. Appl Environ Microbiol 53:2124–2128Google Scholar
  16. Biswas S, Biswas I (2005) Role of HtrA in surface protein expression and biofilm formation by Streptococcus mutans. Infect Immun 73:6923–6934CrossRefGoogle 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. Bradshaw DJ, McKee AS, Marsh PD (1989) Effects of carbohydrate pulses and pH on population shifts within oral microbial communities in vitro. J Dent Res 68:1298–1302CrossRefGoogle Scholar
  19. Broadbent JR, Larsen RL, Deibel V, Steele JL (2010) Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J Bacteriol 192:2445–2458CrossRefGoogle Scholar
  20. Budin-Verneuil A, Maguin E, Auffray Y, Ehrlich SD, Pichereau V (2005a) Transcriptional analysis of the cyclopropane fatty acid synthase gene of Lactococcus lactis MG1363 at low pH. FEMS Microbiol Lett 250:189–194CrossRefGoogle Scholar
  21. Budin-Verneuil A, Pichereau V, Auffray Y, Ehrlich DS, Maguin E (2005b) Proteomic characterization of the acid tolerance response in Lactococcus lactis MG1363. Proteomics 5:4794–4807CrossRefGoogle Scholar
  22. Budin-Verneuil A, Maguin E, Auffray Y, Ehrlich DS, Pichereau V (2006) Genetic structure and transcriptional analysis of the arginine deiminase (ADI) cluster in Lactococcus lactis MG1363. Can J Microbiol 52:617–622CrossRefGoogle Scholar
  23. Budin-Verneuil A, Pichereau V, Auffray Y, Ehrlich D, Maguin E (2007) Proteome phenotyping of acid stress-resistant mutants of Lactococcus lactis MG1363. Proteomics 7:2038–2046CrossRefGoogle Scholar
  24. Burne RA, Parsons DT, Marquis RE (1989) Cloning and expression in Escherichia coli of the genes of the arginine deiminase system of Streptococcus sanguis NCTC 10904. Infect Immun 57:3540–3548Google Scholar
  25. Cappa F, Cattivelli D, Cocconcelli PS (2005) The uvrA gene is involved in oxidative and acid stress responses in Lactobacillus helveticus CNBL1156. Res Microbiol 156:1039–1047CrossRefGoogle Scholar
  26. Casiano-Colon A, Marquis RE (1988) Role of the arginine deiminase system in protecting oral bacteria and an enzymatic basis for acid tolerance. Appl Environ Microbiol 54:1318–1324Google Scholar
  27. Champomier Verges MC, Zuniga M, Morel-Deville F, Perez-Martinez G, Zagorec M, Ehrlich SD (1999) Relationships between arginine degradation, pH and survival in Lactobacillus sakei. FEMS Microbiol Lett 180:297–304CrossRefGoogle Scholar
  28. 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 192:1312–1323CrossRefGoogle Scholar
  29. Chen YY, Burne RA (2003) Identification and characterization of the nickel uptake system for urease biogenesis in Streptococcus salivarius 57.I. J Bacteriol 185:6773–6779CrossRefGoogle Scholar
  30. Chen YY, Weaver CA, Mendelsohn DR, Burne RA (1998) Transcriptional regulation of the Streptococcus salivarius 57.I urease operon. J Bacteriol 180:5769–5775Google Scholar
  31. Chong P, Drake L, Biswas I (2008) LiaS regulates virulence factor expression in Streptococcus mutans. Infect Immun 76:3093–3099CrossRefGoogle Scholar
  32. Cox DJ, Henick-Kling T (1989) Chemiosmotic energy from malolactic fermentation. J Bacteriol 171:5750–5752Google Scholar
  33. Davis CR, Wibowo DJ, Lee TH, Fleet GH (1986) Growth and metabolism of lactic acid bacteria during and after malolactic fermentation of wines at different pH. Appl Environ Microbiol 51:539–545Google Scholar
  34. Denayrolles M, Aigle M, Lonvaud-Funel A (1994) Cloning and sequence analysis of the gene encoding Lactococcus lactis malolactic enzyme: relationships with malic enzymes. FEMS Microbiol Lett 116:79–86CrossRefGoogle Scholar
  35. Duary RK, Batish VK, Grover S (2010) Expression of the atpD gene in probiotic Lactobacillus plantarum strains under in vitro acidic conditions using RT-qPCR. Res Microbiol 161:399–405CrossRefGoogle Scholar
  36. Ehrmann M, Clausen T (2004) Proteolysis as a regulatory mechanism. Annu Rev Genet 38:709–724CrossRefGoogle Scholar
  37. Even S, Lindley ND, Cocaign-Bousquet M (2003) Transcriptional, translational and metabolic regulation of glycolysis in Lactococcus lactis subsp. cremoris MG 1363 grown in continuous acidic cultures. Microbiology (Reading, Engl) 149:1935–1944CrossRefGoogle Scholar
  38. Fenoll A, Munoz R, Garcia E, de la Campa AG (1994) Molecular basis of the optochin-sensitive phenotype of pneumococcus: characterization of the genes encoding the F0 complex of the Streptococcus pneumoniae and Streptococcus oralis H(+)-ATPases. Mol Microbiol 12:587–598CrossRefGoogle Scholar
  39. Fenoll A, Munoz R, Garcia E, de la Campa AG (1995) Optochin sensitivity is encoded by the atpC gene of the Streptococcus pneumonia atp (F0F1 H(+)-ATPase) operon. Dev Biol Stand 85:287–291Google Scholar
  40. Fernandez A, Ogawa J, Penaud S, Boudebbouze S, Ehrlich D, van de Guchte M, Maguin E (2008) Rerouting of pyruvate metabolism during acid adaptation in Lactobacillus bulgaricus. Proteomics 8:3154–3163CrossRefGoogle Scholar
  41. Fozo EM, Quivey RG Jr (2004a) Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol 70:929–936CrossRefGoogle Scholar
  42. 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 186:4152–4158CrossRefGoogle Scholar
  43. Fozo EM, Kajfasz JK, Quivey RG Jr (2004) Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol Lett 238:291–295CrossRefGoogle Scholar
  44. Fozo EM, Scott-Anne K, Koo H, Quivey RG Jr (2007) Role of unsaturated fatty acid biosynthesis in virulence of Streptococcus mutans. Infect Immun 75:1537–1539CrossRefGoogle Scholar
  45. Gao R, Stock AM (2009) Biological insights from structures of two-component proteins. Annu Rev Microbiol 63:133–154CrossRefGoogle Scholar
  46. Griswold AR, Chen YY, Burne RA (2004) Analysis of an agmatine deiminase gene cluster in Streptococcus mutans UA159. J Bacteriol 186:1902–1904CrossRefGoogle Scholar
  47. Griswold AR, Jameson-Lee M, Burne RA (2006) Regulation and physiologic significance of the agmatine deiminase system of Streptococcus mutans UA159. J Bacteriol 188:834–841CrossRefGoogle Scholar
  48. Griswold AR, Nascimento MM, Burne RA (2009) Distribution, regulation and role of the agmatine deiminase system in mutans streptococci. Oral Microbiol Immunol 24:79–82CrossRefGoogle Scholar
  49. Gutierrez JA, Crowley PJ, Cvitkovitch DG, Brady LJ, Hamilton IR, Hillman JD, Bleiweis AS (1999) Streptococcus mutans ffh, a gene encoding a homologue of the 54 kDa subunit of the signal recognition particle, is involved in resistance to acid stress. Microbiology 145(Pt 2):357–366CrossRefGoogle Scholar
  50. Guzzo J, Jobin MP, Delmas F, Fortier LC, Garmyn D, Tourdot-Maréchal R, Lee B, Diviès C (2000) Regulation of stress response in Oenococcus oeni as a function of environmental changes and growth phase. Int J Food Microbiol 55:27–31CrossRefGoogle Scholar
  51. 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 183:5964–5973CrossRefGoogle Scholar
  52. 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 102:17466–17471CrossRefGoogle Scholar
  53. Ingmer H, Brondsted L (2009) Proteases in bacterial pathogenesis. Res Microbiol 160:704–710CrossRefGoogle Scholar
  54. 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 25:329–341CrossRefGoogle Scholar
  55. Jerga A, Rock CO (2009) Acyl-acyl carrier protein regulates transcription of fatty acid biosynthetic genes via the FabT repressor in Streptococcus pneumoniae. J Biol Chem 284:15364–15368CrossRefGoogle Scholar
  56. Kajfasz JK, Martinez AR, Rivera-Ramos I, Abranches J, Koo H, Quivey RG Jr, Lemos JA (2009) Role of Clp proteins in expression of virulence properties of Streptococcus mutans. J Bacteriol 191:2060–2068CrossRefGoogle Scholar
  57. Kang K-h, Lee J-S, Yoo M, Jin I (2010) The influence of HtrA expression on the growth of Streptococcus mutans during acid stress. Mol Cells 29:297–304CrossRefGoogle Scholar
  58. Kawada-Matsuo M, Shibata Y, Yamashita Y (2009) Role of two component signaling response regulators in acid tolerance of Streptococcus mutans. Oral Microbiol Immunol 24:173–176CrossRefGoogle Scholar
  59. Keijser BJ, Zaura E, Huse SM, van der Vossen JM, Schuren FH, Montijn RC, ten Cate JM, Crielaard W (2008) Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res 87:1016–1020CrossRefGoogle Scholar
  60. Klein MI, Duarte S, Xiao J, Mitra S, Foster TH, Koo H (2009) Structural and molecular basis of the role of starch and sucrose in Streptococcus mutans biofilm development. Appl Environ Microbiol 75:837–841CrossRefGoogle Scholar
  61. Konings WN, Lolkema JS, Bolhuis H, van Veen HW, Poolman B, Driessen AJ (1997) The role of transport processes in survival of lactic acid bacteria. Energy transduction and multidrug resistance. Antonie van Leeuwenhoek 71:117–128Google Scholar
  62. Krastel K, Senadheera DB, Mair R, Downey JS, Goodman SD, Cvitkovitch DG (2010) Characterization of a glutamate transporter operon, glnQHMP, in Streptococcus mutans and its role in acid tolerance. J Bacteriol 192:984–993CrossRefGoogle Scholar
  63. Krell T, Lacal J, Busch A, Silva-Jimenez H, Guazzaroni ME, Ramos JL (2010) Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 64:539–559CrossRefGoogle Scholar
  64. Kuhnert WL, Zheng G, Faustoferri RC, Quivey RG Jr (2004) The F-ATPase operon promoter of Streptococcus mutans is transcriptionally regulated in response to external pH. J Bacteriol 186:8524–8528CrossRefGoogle Scholar
  65. Labarre C, Divies C, Guzzo J (1996) Genetic organization of the mle locus and identification of a mleR-like gene from Leuconostoc oenos. Appl Environ Microbiol 62:4493–4498Google Scholar
  66. Lafon-Lafourcade S, Carre E, Ribereau-Gayon P (1983) Occurrence of lactic acid bacteria during the different stages of vinification and conservation of wines. Appl Environ Microbiol 46:874–880Google Scholar
  67. Laport MS, Lemos JA, Bastos Md Mdo C, Burne RA, Giambiagi-De Marval M (2004) Transcriptional analysis of the groE and dnaK heat-shock operons of Enterococcus faecalis. Res Microbiol 155:252–258CrossRefGoogle Scholar
  68. Laport MS, Dos Santos LL, Lemos JA, do Carmo FBM, Burne RA, Giambiagi-Demarval M (2006) Organization of heat shock dnaK and groE operons of the nosocomial pathogen Enterococcus faecium. Res Microbiol 157:162–168Google Scholar
  69. Lee K, Lee H-G, Pi K, Choi Y-J (2008) The effect of low pH on protein expression by the probiotic bacterium Lactobacillus reuteri. Proteomics 8:1624–1630CrossRefGoogle Scholar
  70. Lee K, Pi K (2010) Effect of transient acid stress on the proteome of intestinal probiotic Lactobacillus reuteri. Biochemistry (Mosc) 75:460–465CrossRefGoogle Scholar
  71. Lee K, Pi K, Kim EB, Rho B-S, Kang S-K, Lee HG, Choi Y-J (2010) Glutathione-mediated response to acid stress in the probiotic bacterium, Lactobacillus salivarius. Biotechnol Lett 32:969–972CrossRefGoogle Scholar
  72. Lemme A, Sztajer H, Wagner-Döbler I (2010) Characterization of mleR, a positive regulator of malolactic fermentation and part of the acid tolerance response in Streptococcus mutans. BMC Microbiol 10:58CrossRefGoogle Scholar
  73. Lemos JA, Burne RA (2002) Regulation and physiological significance of ClpC and ClpP in Streptococcus mutans. J Bacteriol 184:6357–6366CrossRefGoogle Scholar
  74. 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 72:1431–1440CrossRefGoogle Scholar
  75. Len ACL, Harty DWS, Jacques NA (2004a) Proteome analysis of Streptococcus mutans metabolic phenotype during acid tolerance. Microbiology (Reading, Engl) 150:1353–1366CrossRefGoogle Scholar
  76. Len ACL, Harty DWS, Jacques NA (2004b) Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance. Microbiology (Reading, Engl) 150:1339–1351CrossRefGoogle Scholar
  77. 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 45:398–404CrossRefGoogle Scholar
  78. Li YH, Chen YY, Burne RA (2000) Regulation of urease gene expression by Streptococcus salivarius growing in biofilms. Environ Microbiol 2:169–177CrossRefGoogle Scholar
  79. Li YH, Lau PC, Tang N, Svensater G, Ellen RP, Cvitkovitch DG (2002) Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans. J Bacteriol 184:6333–6342CrossRefGoogle Scholar
  80. Lim EM, Ehrlich SD, Maguin E (2000) Identification of stress-inducible proteins in Lactobacillus delbrueckii subsp. bulgaricus. Electrophoresis 21:2557–2561CrossRefGoogle Scholar
  81. Liu Y, Burne RA (2009) Multiple two-component systems of Streptococcus mutans regulate agmatine deiminase gene expression and stress tolerance. J Bacteriol 191:7363–7366CrossRefGoogle Scholar
  82. Liu Y, Zeng L, Burne RA (2009) AguR is required for induction of the Streptococcus mutans agmatine deiminase system by low pH and agmatine. Appl Environ Microbiol 75:2629–2637CrossRefGoogle Scholar
  83. Lolkema JS, Poolman B, Konings WN (1995) Role of scalar protons in metabolic energy generation in lactic acid bacteria. J Bioenerg Biomembr 27:467–473CrossRefGoogle Scholar
  84. Lorca GL, Valdez GF (2001) A low-pH-inducible, stationary-phase acid tolerance response in Lactobacillus acidophilus CRL 639. Curr Microbiol 42:21–25CrossRefGoogle Scholar
  85. Lu YJ, Rock CO (2006) Transcriptional regulation of fatty acid biosynthesis in Streptococcus pneumoniae. Mol Microbiol 59:551–566CrossRefGoogle Scholar
  86. Lucas PM, Blancato VS, Claisse O, Magni C, Lolkema JS, Lonvaud-Funel A (2007) Agmatine deiminase pathway genes in Lactobacillus brevis are linked to the tyrosine decarboxylation operon in a putative acid resistance locus. Microbiology 153:2221–2230CrossRefGoogle Scholar
  87. Magnusson LU, Farewell A, Nystrom T (2005) ppGpp: A global regulator in Escherichia coli. Trends Microbiol 13:236–242CrossRefGoogle Scholar
  88. Mangani S, Guerrini S, Granchi L, Vincenzini M (2005) Putrescine accumulation in wine: role of Oenococcus oeni. Curr Microbiol 51:6–10CrossRefGoogle Scholar
  89. Marquis RE, Bender GR, Murray DR, Wong A (1987) Arginine deiminase system and bacterial adaptation to acid environments. Appl Environ Microbiol 53:198–200Google Scholar
  90. Marrakchi H, Choi KH, Rock CO (2002) A new mechanism for anaerobic unsaturated fatty acid formation in Streptococcus pneumoniae. J Biol Chem 277:44809–44816CrossRefGoogle Scholar
  91. Martín MG, Sender PD, Peirú S, de Mendoza D, Magni C (2004) Acid-inducible transcription of the operon encoding the citrate lyase complex of Lactococcus lactis Biovar diacetylactis CRL264. J Bacteriol 186:5649–5660CrossRefGoogle Scholar
  92. Martín-Galiano AJ, Ferrandiz MJ, de la Campa AG (2001) The promoter of the operon encoding the F0F1 ATPase of Streptococcus pneumoniae is inducible by pH. Mol Microbiol 41:1327–1338CrossRefGoogle Scholar
  93. Martín-Galiano AJ, Overweg K, Ferrándiz MJ, Reuter M, Wells JM, de la Campa AG (2005) Transcriptional analysis of the acid tolerance response in Streptococcus pneumoniae. Microbiology (Reading, Engl) 151:3935–3946CrossRefGoogle Scholar
  94. Martinez AR, Abranches J, Kajfasz JK, Lemos JA (2010) Characterization of the Streptococcus sobrinus acid-stress response by interspecies microarrays and proteomics. Mol Oral Microbiol 25:331–342Google Scholar
  95. McDermid AS, McKee AS, Ellwood DC, Marsh PD (1986) The effect of lowering the pH on the composition and metabolism of a community of nine oral bacteria grown in a chemostat. J Gen Microbiol 132:1205–1214Google Scholar
  96. McKee AS, McDermid AS, Ellwood DC, Marsh PD (1985) The establishment of reproducible, complex communities of oral bacteria in the chemostat using defined inocula. J Appl Bacteriol 59:263–275Google Scholar
  97. McNeill K, Hamilton IR (2004) Effect of acid stress on the physiology of biofilm cells of Streptococcus mutans. Microbiology (Reading, Engl) 150:735–742CrossRefGoogle Scholar
  98. Mercade M, Cocaign-Bousquet M, Loubière P (2006) Glyceraldehyde-3-phosphate dehydrogenase regulation in Lactococcus lactis ssp. cremoris MG1363 or relA mutant at low pH. J Appl Microbiol 100:1364–1372CrossRefGoogle Scholar
  99. Montanari C, Sado Kamdem SL, Serrazanetti DI, Etoa F-X, Guerzoni ME (2010) Synthesis of cyclopropane fatty acids in Lactobacillus helveticus and Lactobacillus sanfranciscensis and their cellular fatty acids changes following short term acid and cold stresses. Food Microbiol 27:493–502CrossRefGoogle Scholar
  100. Mora D, Monnet C, Parini C, Guglielmetti S, Mariani A, Pintus P, Molinari F, Daffonchio D, Manachini PL (2005) Urease biogenesis in Streptococcus thermophilus. Res Microbiol 156:897–903CrossRefGoogle Scholar
  101. Morello E, Bermudez-Humaran LG, Llull D, Sole V, Miraglio N, Langella P, Poquet I (2008) Lactococcus lactis, an efficient cell factory for recombinant protein production and secretion. J Mol Microbiol Biotechnol 14:48–58CrossRefGoogle Scholar
  102. Munoz R, Garcia E, De la Campa AG (1996) Quinine specifically inhibits the proteolipid subunit of the F0F1 H  +  -ATPase of Streptococcus pneumoniae. J Bacteriol 178:2455–2458Google Scholar
  103. Nascimento MM, Lemos JA, Abranches J, Goncalves RB, Burne RA (2004) Adaptive acid tolerance response of Streptococcus sobrinus. J Bacteriol 186:6383–6390CrossRefGoogle Scholar
  104. Nascimento MM, Gordan VV, Garvan CW, Browngardt CM, Burne RA (2009) Correlations of oral bacterial arginine and urea catabolism with caries experience. Oral Microbiol Immunol 24:89–95CrossRefGoogle Scholar
  105. Oberreuter H, Mertens F, Seiler H, Scherer S (2000) Quantification of micro-organisms in binary mixed populations by Fourier transform infrared (FT-IR) spectroscopy. Lett Appl Microbiol 30:85–89CrossRefGoogle Scholar
  106. Pallen MJ, Wren BW (1997) The HtrA family of serine proteases. Mol Microbiol 26:209–221CrossRefGoogle Scholar
  107. 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 73:465–476CrossRefGoogle Scholar
  108. Papadimitriou K, Boutou E, Zoumpopoulou 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 74:6068–6076CrossRefGoogle Scholar
  109. Pernoud S, Fremaux C, Sepulchre A, Corrieu G, Monnet C (2004) Effect of the metabolism of urea on the acidifying activity of Streptococcus thermophilus. J Dairy Sci 87:550–555CrossRefGoogle Scholar
  110. Pieterse B, Leer RJ, Schuren FHJ, van der Werf MJ (2005) Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. Microbiology (Reading, Engl) 151:3881–3894CrossRefGoogle Scholar
  111. Pilone GJ, Kunkee RE (1970) Carbonic acid from decarboxylation by “malic” enzyme in lactic acid bacteria. J Bacteriol 103:404–409Google Scholar
  112. Poolman B, Driessen AJ, Konings WN (1987) Regulation of arginine-ornithine exchange and the arginine deiminase pathway in Streptococcus lactis. J Bacteriol 169:5597–5604Google Scholar
  113. Poolman B, Molenaar D, Smid EJ, Ubbink T, Abee T, Renault PP, Konings WN (1991) Malolactic fermentation: electrogenic malate uptake and malate/lactate antiport generate metabolic energy. J Bacteriol 173:6030–6037Google Scholar
  114. Potrykus K, Cashel M (2008) (p)ppGpp: Still magical? Annu Rev Microbiol 62:35–51CrossRefGoogle Scholar
  115. Quivey RG Jr, Faustoferri RC, Clancy KA, Marquis RE (1995) Acid adaptation in Streptococcus mutans UA159 alleviates sensitization to environmental stress due to RecA deficiency. FEMS Microbiol Lett 126:257–261CrossRefGoogle Scholar
  116. 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 189:89–92CrossRefGoogle Scholar
  117. Rallu F, Gruss A, Maguin E (1996) Lactococcus lactis and stress. Antonie van Leeuwenhoek 70:243–251CrossRefGoogle Scholar
  118. Rallu F, Gruss A, Ehrlich SD, Maguin E (2000) Acid- and multistress-resistant mutants of Lactococcus lactis: identification of intracellular stress signals. Mol Microbiol 35:517–528CrossRefGoogle Scholar
  119. Renault P, Gaillardin C, Heslot H (1988) Role of malolactic fermentation in lactic acid bacteria. Biochimie 70:375–379CrossRefGoogle Scholar
  120. Renault P, Gaillardin C, Heslot H (1989) Product of the Lactococcus lactis gene required for malolactic fermentation is homologous to a family of positive regulators. J Bacteriol 171:3108–3114Google Scholar
  121. Salema M, Poolman B, Lolkema JS, Dias MC, Konings WN (1994) Uniport of monoanionic L-malate in membrane vesicles from Leuconostoc oenos. Eur J Biochem 225:289–295CrossRefGoogle Scholar
  122. Salema M, Capucho I, Poolman B, San Romao MV, Dias MC (1996) In vitro reassembly of the malolactic fermentation pathway of Leuconostoc oenos (Oenococcus oeni). J Bacteriol 178:5537–5539Google Scholar
  123. Sánchez C, Neves AR, Cavalheiro J, dos Santos MM, García-Quintáns N, López P, Santos H (2008) Contribution of citrate metabolism to the growth of Lactococcus lactis CRL264 at low pH. Appl Environ Microbiol 74:1136–1144CrossRefGoogle Scholar
  124. Santi I, Grifantini R, Jiang S-M, 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 191:5387–5397CrossRefGoogle Scholar
  125. 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 191:6415–6424CrossRefGoogle Scholar
  126. Senadheera MD, Guggenheim B, Spatafora GA, Huang YC, Choi J, Hung DC, Treglown JS, Goodman SD, Ellen RP, Cvitkovitch DG (2005) A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. J Bacteriol 187:4064–4076CrossRefGoogle Scholar
  127. Sheng J, Marquis RE (2007) Malolactic fermentation by Streptococcus mutans. FEMS Microbiol Lett 272:196–201CrossRefGoogle Scholar
  128. Sheng J, Baldeck JD, Nguyen PT, Quivey RG Jr, Marquis RE (2010) Alkali production associated with malolactic fermentation by oral streptococci and protection against acid, oxidative, or starvation damage. Can J Microbiol 56:539–547CrossRefGoogle Scholar
  129. Shu M, Browngardt CM, Chen YY, Burne RA (2003) Role of urease enzymes in stability of a 10-species oral biofilm consortium cultivated in a constant-depth film fermenter. Infect Immun 71:7188–7192CrossRefGoogle Scholar
  130. Shu M, Morou-Bermudez E, Suarez-Perez E, Rivera-Miranda C, Browngardt CM, Chen YY, Magnusson I, Burne RA (2007) The relationship between dental caries status and dental plaque urease activity. Oral Microbiol Immunol 22:61–66CrossRefGoogle Scholar
  131. Small PL, Waterman SR (1998) Acid stress, anaerobiosis and gadCB: lessons from Lactococcus lactis and Escherichia coli. Trends Microbiol 6:214–216CrossRefGoogle Scholar
  132. Smith AJ, Quivey RG Jr, Faustoferri RC (1996) Cloning and nucleotide sequence analysis of the Streptococcus mutans membrane-bound, proton-translocating ATPase operon. Gene 183:87–96CrossRefGoogle Scholar
  133. 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
  134. Svensater G, Sjogreen B, Hamilton IR (2000) Multiple stress responses in Streptococcus mutans and the induction of general and stress-specific proteins. Microbiology 146(Pt 1):107–117Google Scholar
  135. Svensater G, Welin J, Wilkins JC, Beighton D, Hamilton IR (2001) Protein expression by planktonic and biofilm cells of Streptococcus mutans. FEMS Microbiol Lett 205:139–146CrossRefGoogle Scholar
  136. Tonon T, Lonvaud-Funel A (2000) Metabolism of arginine and its positive effect on growth and revival of Oenococcus oeni. J Appl Microbiol 89:526–531CrossRefGoogle Scholar
  137. Toro E, Nascimento MM, Suarez-Perez E, Burne RA, Elias-Boneta A, Morou-Bermudez E (2010) The effect of sucrose on plaque and saliva urease levels in vivo. Arch Oral Biol 55:249–254CrossRefGoogle Scholar
  138. Traxler MF, Summers SM, Nguyen HT, Zacharia VM, Hightower GA, Smith JT, Conway T (2008) The global, ppGpp-mediated stringent response to amino acid starvation in Escherichia coli. Mol Microbiol 68:1128–1148CrossRefGoogle Scholar
  139. Vrancken G, Rimaux T, Weckx S, De Vuyst L, Leroy F (2009a) Environmental pH determines citrulline and ornithine release through the arginine deiminase pathway in Lactobacillus fermentum IMDO 130101. Int J Food Microbiol 135:216–222CrossRefGoogle Scholar
  140. Vrancken G, Rimaux T, Wouters D, Leroy F, De Vuyst L (2009b) The arginine deiminase pathway of Lactobacillus fermentum IMDO 130101 responds to growth under stress conditions of both temperature and salt. Food Microbiol 26:720–727CrossRefGoogle Scholar
  141. Walker DC, Girgis HS, Klaenhammer TR (1999) The groESL chaperone operon of Lactobacillus johnsonii. Appl Environ Microbiol 65:3033–3041Google Scholar
  142. Walker JE, Saraste M, Gay NJ (1984) The unc operon. Nucleotide sequence, regulation and structure of ATP-synthase. Biochim Biophys Acta 768:164–200Google Scholar
  143. Wall T, Båth K, Britton RA, Jonsson H, Versalovic J, Roos S (2007) The early response to acid shock in Lactobacillus reuteri involves the ClpL chaperone and a putative cell wall-altering esterase. Appl Environ Microbiol 73:3924–3935CrossRefGoogle Scholar
  144. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63CrossRefGoogle Scholar
  145. Welin J, Wilkins JC, Beighton D, Svensater G (2004) Protein expression by Streptococcus mutans during initial stage of biofilm formation. Appl Environ Microbiol 70:3736–3741CrossRefGoogle Scholar
  146. Welin-Neilands J, Svensäter G (2007) Acid tolerance of biofilm cells of Streptococcus mutans. Appl Environ Microbiol 73:5633–5638CrossRefGoogle Scholar
  147. Wilkins JC, Homer KA, Beighton D (2001) Altered protein expression of Streptococcus oralis cultured at low pH revealed by two-dimensional gel electrophoresis. Appl Environ Microbiol 67:3396–3405CrossRefGoogle Scholar
  148. Xie Y, Chou L-S, Cutler A, Weimer B (2004) DNA macroarray profiling of Lactococcus lactis subsp. lactis IL1403 gene expression during environmental stresses. Appl Environ Microbiol 70:6738–6747CrossRefGoogle Scholar
  149. Zhang J, Fu R-Y, Hugenholtz J, Li Y, Chen J (2007) Glutathione protects Lactococcus lactis against acid stress. Appl Environ Microbiol 73:5268–5275CrossRefGoogle Scholar
  150. Zhang J, Banerjee A, Biswas I (2009) Transcription of clpP is enhanced by a unique tandem repeat sequence in Streptococcus mutans. J Bacteriol 191:1056–1065CrossRefGoogle Scholar
  151. Zhu Q, Quivey RG Jr, Berger AJ (2004) Measurement of bacterial concentration fractions in polymicrobial mixtures by Raman microspectroscopy. J Biomed Opt 9:1182–1186CrossRefGoogle Scholar
  152. Zhu Q, Quivey RG Jr, Berger AJ (2007) Raman spectroscopic measurement of relative concentrations in mixtures of oral bacteria. Appl Spectrosc 61:1233–1237CrossRefGoogle Scholar
  153. Zuniga M, Miralles Md Mdel C, Perez-Martinez G (2002) The Product of arcR, the sixth gene of the arc operon of Lactobacillus sakei, is essential for expression of the arginine deiminase pathway. Appl Environ Microbiol 68:6051–6058CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Center for Oral BiologyUniversity of Rochester, School of Medicine and DentistryRochesterUSA
  2. 2.Center for Oral BiologyUniversity of Rochester, School of Medicine and DentistryRochesterUSA
  3. 3.Department of Microbiology and ImmunologyUniversity of Rochester, School of Medicine and DentistryRochesterUSA

Personalised recommendations