Abstract
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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
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 46:1407–1417
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 99:14434–14439
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 332:74–80
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 57:1841–1847
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 301:61–66
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 70:5315–5322
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 272:18140–18146
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 40:1001–1009
Beier BD, Quivey RGJ, Berger AJ (2010) Identification of different bacterial species in biofilms using confocal raman microscopy. J Biomed Opt 15(6):066001
Belli WA, Marquis RE (1991) Adaptation of Streptococcus mutans and Enterococcus hirae to acid stress in continuous culture. Appl Environ Microbiol 57:1134–1138
Belli WA, Marquis RE (1994) Catabolite modification of acid tolerance of Streptococcus mutans GS-5. Oral Microbiol Immunol 9:29–34
Belli WA, Buckley DH, Marquis RE (1995) Weak acid effects and fluoride inhibition of glycolysis by Streptococcus mutans GS-5. Can J Microbiol 41:785–791
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 186:2200–2205
Bender GR, Sutton SV, Marquis RE (1986) Acid tolerance, proton permeabilities, and membrane ATPases of oral streptococci. Infect Immun 53:331–338
Bender GR, Marquis RE (1987) Membrane ATPases and acid tolerance of Actinomyces viscosus and Lactobacillus casei. Appl Environ Microbiol 53:2124–2128
Biswas S, Biswas I (2005) Role of HtrA in surface protein expression and biofilm formation by Streptococcus mutans. Infect Immun 73:6923–6934
Biswas I, Drake L, Erkina D, Biswas S (2008) Involvement of sensor kinases in the stress tolerance response of Streptococcus mutans. J Bacteriol 190:68–77
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 68:1298–1302
Broadbent JR, Larsen RL, Deibel V, Steele JL (2010) Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J Bacteriol 192:2445–2458
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 250:189–194
Budin-Verneuil A, Pichereau V, Auffray Y, Ehrlich DS, Maguin E (2005b) Proteomic characterization of the acid tolerance response in Lactococcus lactis MG1363. Proteomics 5:4794–4807
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 52:617–622
Budin-Verneuil A, Pichereau V, Auffray Y, Ehrlich D, Maguin E (2007) Proteome phenotyping of acid stress-resistant mutants of Lactococcus lactis MG1363. Proteomics 7:2038–2046
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 57:3540–3548
Cappa F, Cattivelli D, Cocconcelli PS (2005) The uvrA gene is involved in oxidative and acid stress responses in Lactobacillus helveticus CNBL1156. Res Microbiol 156:1039–1047
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 54:1318–1324
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 180:297–304
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 192:1312–1323
Chen YY, Burne RA (2003) Identification and characterization of the nickel uptake system for urease biogenesis in Streptococcus salivarius 57.I. J Bacteriol 185:6773–6779
Chen YY, Weaver CA, Mendelsohn DR, Burne RA (1998) Transcriptional regulation of the Streptococcus salivarius 57.I urease operon. J Bacteriol 180:5769–5775
Chong P, Drake L, Biswas I (2008) LiaS regulates virulence factor expression in Streptococcus mutans. Infect Immun 76:3093–3099
Cox DJ, Henick-Kling T (1989) Chemiosmotic energy from malolactic fermentation. J Bacteriol 171:5750–5752
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 51:539–545
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 116:79–86
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 161:399–405
Ehrmann M, Clausen T (2004) Proteolysis as a regulatory mechanism. Annu Rev Genet 38:709–724
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) 149:1935–1944
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 12:587–598
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 85:287–291
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 8:3154–3163
Fozo EM, Quivey RG Jr (2004a) Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol 70:929–936
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 186:4152–4158
Fozo EM, Kajfasz JK, Quivey RG Jr (2004) Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol Lett 238:291–295
Fozo EM, Scott-Anne K, Koo H, Quivey RG Jr (2007) Role of unsaturated fatty acid biosynthesis in virulence of Streptococcus mutans. Infect Immun 75:1537–1539
Gao R, Stock AM (2009) Biological insights from structures of two-component proteins. Annu Rev Microbiol 63:133–154
Griswold AR, Chen YY, Burne RA (2004) Analysis of an agmatine deiminase gene cluster in Streptococcus mutans UA159. J Bacteriol 186:1902–1904
Griswold AR, Jameson-Lee M, Burne RA (2006) Regulation and physiologic significance of the agmatine deiminase system of Streptococcus mutans UA159. J Bacteriol 188:834–841
Griswold AR, Nascimento MM, Burne RA (2009) Distribution, regulation and role of the agmatine deiminase system in mutans streptococci. Oral Microbiol Immunol 24:79–82
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):357–366
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 55:27–31
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 183:5964–5973
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 102:17466–17471
Ingmer H, Brondsted L (2009) Proteases in bacterial pathogenesis. Res Microbiol 160:704–710
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 25:329–341
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 284:15364–15368
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 191:2060–2068
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 29:297–304
Kawada-Matsuo M, Shibata Y, Yamashita Y (2009) Role of two component signaling response regulators in acid tolerance of Streptococcus mutans. Oral Microbiol Immunol 24:173–176
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 87:1016–1020
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 75:837–841
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 71:117–128
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 192:984–993
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 64:539–559
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 186:8524–8528
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 62:4493–4498
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 46:874–880
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 155:252–258
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 157:162–168
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 8:1624–1630
Lee K, Pi K (2010) Effect of transient acid stress on the proteome of intestinal probiotic Lactobacillus reuteri. Biochemistry (Mosc) 75:460–465
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 32:969–972
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 10:58
Lemos JA, Burne RA (2002) Regulation and physiological significance of ClpC and ClpP in Streptococcus mutans. J Bacteriol 184:6357–6366
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 72:1431–1440
Len ACL, Harty DWS, Jacques NA (2004a) Proteome analysis of Streptococcus mutans metabolic phenotype during acid tolerance. Microbiology (Reading, Engl) 150:1353–1366
Len ACL, Harty DWS, Jacques NA (2004b) Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance. Microbiology (Reading, Engl) 150:1339–1351
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 45:398–404
Li YH, Chen YY, Burne RA (2000) Regulation of urease gene expression by Streptococcus salivarius growing in biofilms. Environ Microbiol 2:169–177
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 184:6333–6342
Lim EM, Ehrlich SD, Maguin E (2000) Identification of stress-inducible proteins in Lactobacillus delbrueckii subsp. bulgaricus. Electrophoresis 21:2557–2561
Liu Y, Burne RA (2009) Multiple two-component systems of Streptococcus mutans regulate agmatine deiminase gene expression and stress tolerance. J Bacteriol 191:7363–7366
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 75:2629–2637
Lolkema JS, Poolman B, Konings WN (1995) Role of scalar protons in metabolic energy generation in lactic acid bacteria. J Bioenerg Biomembr 27:467–473
Lorca GL, Valdez GF (2001) A low-pH-inducible, stationary-phase acid tolerance response in Lactobacillus acidophilus CRL 639. Curr Microbiol 42:21–25
Lu YJ, Rock CO (2006) Transcriptional regulation of fatty acid biosynthesis in Streptococcus pneumoniae. Mol Microbiol 59:551–566
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 153:2221–2230
Magnusson LU, Farewell A, Nystrom T (2005) ppGpp: A global regulator in Escherichia coli. Trends Microbiol 13:236–242
Mangani S, Guerrini S, Granchi L, Vincenzini M (2005) Putrescine accumulation in wine: role of Oenococcus oeni. Curr Microbiol 51:6–10
Marquis RE, Bender GR, Murray DR, Wong A (1987) Arginine deiminase system and bacterial adaptation to acid environments. Appl Environ Microbiol 53:198–200
Marrakchi H, Choi KH, Rock CO (2002) A new mechanism for anaerobic unsaturated fatty acid formation in Streptococcus pneumoniae. J Biol Chem 277:44809–44816
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 186:5649–5660
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 41:1327–1338
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) 151:3935–3946
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 25:331–342
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 132:1205–1214
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 59:263–275
McNeill K, Hamilton IR (2004) Effect of acid stress on the physiology of biofilm cells of Streptococcus mutans. Microbiology (Reading, Engl) 150:735–742
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 100:1364–1372
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 27:493–502
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 156:897–903
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 14:48–58
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 178:2455–2458
Nascimento MM, Lemos JA, Abranches J, Goncalves RB, Burne RA (2004) Adaptive acid tolerance response of Streptococcus sobrinus. J Bacteriol 186:6383–6390
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 24:89–95
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 30:85–89
Pallen MJ, Wren BW (1997) The HtrA family of serine proteases. Mol Microbiol 26:209–221
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 73:465–476
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 74:6068–6076
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 87:550–555
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) 151:3881–3894
Pilone GJ, Kunkee RE (1970) Carbonic acid from decarboxylation by “malic” enzyme in lactic acid bacteria. J Bacteriol 103:404–409
Poolman B, Driessen AJ, Konings WN (1987) Regulation of arginine-ornithine exchange and the arginine deiminase pathway in Streptococcus lactis. J Bacteriol 169:5597–5604
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 173:6030–6037
Potrykus K, Cashel M (2008) (p)ppGpp: Still magical? Annu Rev Microbiol 62:35–51
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 126:257–261
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 189:89–92
Rallu F, Gruss A, Maguin E (1996) Lactococcus lactis and stress. Antonie van Leeuwenhoek 70:243–251
Rallu F, Gruss A, Ehrlich SD, Maguin E (2000) Acid- and multistress-resistant mutants of Lactococcus lactis: identification of intracellular stress signals. Mol Microbiol 35:517–528
Renault P, Gaillardin C, Heslot H (1988) Role of malolactic fermentation in lactic acid bacteria. Biochimie 70:375–379
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 171:3108–3114
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 225:289–295
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 178:5537–5539
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 74:1136–1144
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 191:5387–5397
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 191:6415–6424
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 187:4064–4076
Sheng J, Marquis RE (2007) Malolactic fermentation by Streptococcus mutans. FEMS Microbiol Lett 272:196–201
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 56:539–547
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 71:7188–7192
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 22:61–66
Small PL, Waterman SR (1998) Acid stress, anaerobiosis and gadCB: lessons from Lactococcus lactis and Escherichia coli. Trends Microbiol 6:214–216
Smith AJ, Quivey RG Jr, Faustoferri RC (1996) Cloning and nucleotide sequence analysis of the Streptococcus mutans membrane-bound, proton-translocating ATPase operon. Gene 183:87–96
Sturr MG, Marquis RE (1992) Comparative acid tolerances and inhibitor sensitivities of isolated F-ATPases of oral lactic acid bacteria. Appl Environ Microbiol 58:2287–2291
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):107–117
Svensater G, Welin J, Wilkins JC, Beighton D, Hamilton IR (2001) Protein expression by planktonic and biofilm cells of Streptococcus mutans. FEMS Microbiol Lett 205:139–146
Tonon T, Lonvaud-Funel A (2000) Metabolism of arginine and its positive effect on growth and revival of Oenococcus oeni. J Appl Microbiol 89:526–531
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 55:249–254
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 68:1128–1148
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 135:216–222
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 26:720–727
Walker DC, Girgis HS, Klaenhammer TR (1999) The groESL chaperone operon of Lactobacillus johnsonii. Appl Environ Microbiol 65:3033–3041
Walker JE, Saraste M, Gay NJ (1984) The unc operon. Nucleotide sequence, regulation and structure of ATP-synthase. Biochim Biophys Acta 768:164–200
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 73:3924–3935
Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63
Welin J, Wilkins JC, Beighton D, Svensater G (2004) Protein expression by Streptococcus mutans during initial stage of biofilm formation. Appl Environ Microbiol 70:3736–3741
Welin-Neilands J, Svensäter G (2007) Acid tolerance of biofilm cells of Streptococcus mutans. Appl Environ Microbiol 73:5633–5638
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 67:3396–3405
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 70:6738–6747
Zhang J, Fu R-Y, Hugenholtz J, Li Y, Chen J (2007) Glutathione protects Lactococcus lactis against acid stress. Appl Environ Microbiol 73:5268–5275
Zhang J, Banerjee A, Biswas I (2009) Transcription of clpP is enhanced by a unique tandem repeat sequence in Streptococcus mutans. J Bacteriol 191:1056–1065
Zhu Q, Quivey RG Jr, Berger AJ (2004) Measurement of bacterial concentration fractions in polymicrobial mixtures by Raman microspectroscopy. J Biomed Opt 9:1182–1186
Zhu Q, Quivey RG Jr, Berger AJ (2007) Raman spectroscopic measurement of relative concentrations in mixtures of oral bacteria. Appl Spectrosc 61:1233–1237
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 68:6051–6058
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Kajfasz, J.K., Quivey, R.G. (2011). Responses of Lactic Acid Bacteria to Acid Stress. In: Tsakalidou, E., Papadimitriou, K. (eds) Stress Responses of Lactic Acid Bacteria. Food Microbiology and Food Safety. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-92771-8_2
Download citation
DOI: https://doi.org/10.1007/978-0-387-92771-8_2
Published:
Publisher Name: Springer, Boston, MA
Print ISBN: 978-0-387-92770-1
Online ISBN: 978-0-387-92771-8
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)