Skip to main content
Log in

Stress responses in lactic acid bacteria

  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Lactic acid bacteria (LAB) constitute a heterogeneous group of bacteria that are traditionally used to produce fermented foods. The industrialization of food bio-transformations increased the economical importance of LAB, as they play a crucial role in the development of the organoleptique and hygienic quality of fermented products. Therefore, the reliability of starter strains in terms of quality and functional properties (important for the development of aroma and texture), but also in terms of growth performance and robustness has become essential. These strains should resist to adverse conditions encountered in industrial processes, for example during starter handling and storage (freeze-drying, freezing or spray-drying). The development of new applications such as life vaccines and probiotic foods reinforces the need for robust LAB since they may have to survive in the digestive tract, resist the intestinal flora, maybe colonize the digestive or uro-genital mucosa and express specific functions under conditions that are unfavorable to growth (for example, during stationary phase or storage). Also in nature, the ability to quickly respond to stress is essential for survival and it is now well established that LAB, like other bacteria, evolved defense mechanisms against stress that allow them to withstand harsh conditions and sudden environmental changes. While genes implicated in stress responses are numerous, in LAB the levels of characterization of their actual role and regulation differ widely between species. The functional conservation of several stress proteins (for example, HS proteins, Csp, etc) and of some of their regulators (for example, HrcA, CtsR) renders even more striking the differences that exist between LAB and the classical model micro-organisms. Among the differences observed between LAB species and B. subtilis, one of the most striking is the absence of a σB orthologue in L. lactis ssp. lactisas well as in at least two streptococci and probably E. faecalis. The overview of LAB stress responses also reveals common aspects of stress responses. As in other bacteria, adaptive responses appear to be a usual mode of stress protection in LAB. However, the cross-protection to other stress often induced by the expression of a given adaptive response, appears to vary between species. This observation suggests that the molecular bases of adaptive responses are, at least in part, species (or even subspecies) specific. A better understanding of the mechanisms of stress resistance should allow to understand the bases of the adaptive responses and cross protection, and to rationalize their exploitation to prepare LAB to industrial processes. Moreover, the identification of crucial stress related genes will reveal targets i) for specific manipulation (to promote or limit growth) , ii) to develop tools to screen for tolerant or sensitive strains and iii) to evaluate the fitness and level of adaptation of a culture. In this context, future genome and transcriptome analyses will undoubtedly complement the proteome and genetic information available today, and shed a new light on the perception of, and the response to, stress by lactic acid bacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abdelal A T (1979) Arginine catabolism by microorganisms. Annu Rev Microbiol. 33: 139–168.

    Google Scholar 

  • Abe K, Hayashi H& Maloney P C (1996) Exchange of aspartate and alanine: machanism for development of a proton-motive force in bacteria. J. Biol. Chem. 271: 3079–3084.

    Google Scholar 

  • Adamowicz M, Kelley P M& Nickerson K W (1991) Detergent (sodium dodecyl sulfate) shock proteins in Escherichia coli. J. Bacteriol. 173: 229–233.

    Google Scholar 

  • Archibald F S& Fridovich I (1981) Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria. J Bacteriol. 146: 928–936.

    Google Scholar 

  • Arena M E, Saguir F M& Manca de Nadra M C (1999) Arginine, citrulline and ornithine metabolism by lactic acid bacteria from wine. Int. J. Food Microbiol. 52: 155–161.

    Google Scholar 

  • Arikado E, Ishihara H, Ehara T, Shibata C, Saito H, Kakegawa T, Igarashi K& Kobayashi H (1999) Enzyme level of enterococcal F1Fo-ATPase is regulated by pH at the step of assembly. Eur. J. Biochem. 259: 262–268.

    Google Scholar 

  • Arnau J, Sorensen K I, Appel K F, Vogensen F K& Hammer K (1996) Analysis of heat shock gene expression in Lactococcus lactis MG1363. Microbiology 142: 1685–1691.

    Google Scholar 

  • Auffray Y, Gansel X, Thammavongs B& Boutibonnes P (1992) Heat-shock induced protein synthesis in Lactococcus lactis subsp. lactis. Curr. Microbiol. 24: 281–284.

    Google Scholar 

  • Baati L, Fabre-Gea C, Auriol D& Blanc P J (2000) Study of the cryotolerance of Lactobacillus acidophilus: effect of culture and freezing conditions on the viability and cellular protein levels. Int. J. Food Microbiol. 59: 241–247.

    Google Scholar 

  • Bae W, Jones P G& Inouye M (1997) CspA, the major cold shock protein of Escherichia coli, negatively regulates its own gene expression. J. Bacteriol. 179: 7081–7088.

    Google Scholar 

  • Bae W, Xia B, Inouye M& Severinov K (2000) Escherichia coli CspA-family RNA chaperones are transcription antiterminators. Proc. Natl. Acad. Sci. U.S.A. 97: 7784–7789.

    Google Scholar 

  • Baev D, England R& Kuramitsu H K (1999) Stress-induced membrane association of the Streptococcus mutans GTP-binding protein, an essential G protein, and investigation of its physiological role by utilizing an antisense RNA strategy. Infect Immun. 67: 4510–4516.

    Google Scholar 

  • Bakker E P& Harold F M (1980) Energy coupling to potassium transport in Streptococcus faecalis. J. Biol. Chem. 255: 433–440.

    Google Scholar 

  • Becker G, Klauck E& Hengge-Aronis R (1999) Regulation of RpoS proteolysis in Escherichia coli: the response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc. Natl. Acad. Sci. U.S.A. 96: 6439–6444.

    Google Scholar 

  • Belli W A & Marquis R E (1991) Adapation of Strepococcus mutans and Enteroccus hirae to acid stress in continuous culture. Appl. Environ. Microbiol. 57: 1134–1138.

    Google Scholar 

  • Bernhardt J, Volker U, Volker A, Antelmann H, Schmid R, Mach H& Hecker M (1997) Specific and general stress proteins in Bacillus subtilis-a two-dimensional protein electrophoresis study. Microbiology 143: 999–1017.

    Google Scholar 

  • Blank L M, Koebmann B J, Michelsen O, Nielsen L K& Jensen P R (2001) Hemin reconstitutes proton extrusion in an H(+)-ATPasenegative mutant of Lactococcus lactis. J. Bacteriol. 183: 6707–6709.

    Google Scholar 

  • Bolhuis H, Molenaar D, Poelarends G, van Veen H W, Poolman B, Driessen A J& Konings W N (1994) Proton motive forcedriven and ATP-dependent drug extrusion systems in multidrugresistant Lactococcus lactis. J Bacteriol. 176: 6957–6964.

    Google Scholar 

  • Bolotin A, Mauger S, Malarme K, Ehrlich S D& Sorokin A (1999) Low-redundancy sequencing of the entire Lactococcus lactis IL1403 genome. Antonie Van Leeuwenhoek 76: 27–76.

    Google Scholar 

  • Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich S D& Sorokin A (2001) The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res. 11: 1–23.

    Google Scholar 

  • Bond D R& Russell J B (1996) A role for fructose 1,6-diphosphate in the ATPase-mediated energy spilling reaction of Streptococcus bovis. Appl. Environ. Microbiol. 62: 2095–2099.

    Google Scholar 

  • Bouvier J, Bordes P, Romeo Y, Fourcans A, Bouvier I& Gutierrez C (2000) Characterization of OpuA, a glycine-betaine uptake system of Lactococcus lactis. J. Mol. Microbiol. Biotechnol. 2: 199–205.

    Google Scholar 

  • Boyd D A, Cvitkovitch D G, Bleiweis A S, Kiriukhin M Y, Debabov D V, Neuhaus F C& Hamilton I R (2000) Defects in D-alanyllipoteichoic acid synthesis in Streptococcus mutans results in acid sensitivity. J. Bacteriol. 182: 6055–6065.

    Google Scholar 

  • Brandi A, Pietroni P, Gualerzi C O& Pon C L (1996) Posttranscriptional regulation of CspA expression in Escherichia coli. Mol. Microbiol. 19: 231–240.

    Google Scholar 

  • Breeuwer P, Drocourt J-L, Rombouts F M& Abee T (1996) A novel method for coninuous determination of the intracellular pH in bacteria with the internally conjugated fluorescent probe (and 6) carboxyfluorescein succinimidyl ester. Appl. Environ. Microbiol. 62: 178–183.

    Google Scholar 

  • Broadbent J R& Lin C (1999) Effect of heat shock or cold shock treatment on the resistance of lactococcus lactis to freezing and lyophilization. Cryobiology 39: 88–102.

    Google Scholar 

  • Broadbent J R, Oberg C J& Wei L (1998) Characterization of the Lactobacillus helveticus groESL operon. Res. Microbiol. 149: 247–253.

    Google Scholar 

  • Caldon C E, Yoong P& March P E (2001) Evolution of a molecular switch: universal bacterial GTPases regulate ribosome function. Mol. Microbiol. 41: 289–297.

    Google Scholar 

  • Cashel M, Gentry D, Hernandez V J& Vinella D (1996) The stringent response. In: Neidhardt F C, Ingraham J L, Low K B, Magasanik B, Schaechter M& Umberger H E (eds.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology (pp 1458–1496). American Society for Microbiology Press, Washington, DC.

    Google Scholar 

  • Champomier-Verges M C, Zuniga M, Morel-Deville F, Perez-Martinez G, Zagorec M& Ehrlich S D (1999) Relationships between arginine degradation, pH and survival in Lactobacillus sakei. FEMS Microbiol. Lett. 180: 297–304.

    Google Scholar 

  • Champomier-Verges M C, Chaillou S, Cornet M& Zagorec M (2001) Lactobacillus sakei: recent developments and future prospects. Res. Microbiol. 152: 839–848.

    Google Scholar 

  • Champomier-Verges M C, Maguin E, Mistou M Y, Anglade P&Chich J F (2002) Lactic acid bacteria and proteomics: current knowledge and perspectives. J. Chromatogr. (in press).

  • Chang Y Y& Cronan Jr. J E, (1999) Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol. Microbiol. 33: 249–259.

    Google Scholar 

  • Chapot-Chartier M P, Schouler C, Lepeuple A S, Gripon J C& Chopin M C (1997) Characterization of cspB, a cold-shockinducible gene from Lactococcus lactis, and evidence for a family of genes homologous to the Escherichia coli cspA major cold shock gene. J. Bacteriol. 179: 5589–5593.

    Google Scholar 

  • Chastanet A, Prudhomme M, Claverys J P& Msadek T (2001) Regulation of Streptococcus pneumoniae clp genes and their role in competence development and stress survival. J. Bacteriol. 183: 7295–7307.

    Google Scholar 

  • Chatterji D& Ojha A K (2001) Revisiting the stringent response, ppGpp and starvation signaling. Curr. Opin. Microbiol. 4: 160–165.

    Google Scholar 

  • Chen Y Y& Burne R A (1996) Analysis of Streptococcus salivarius urease expression using continuous chemostat culture. FEMS Microbiol. Lett. 135: 223–229.

    Google Scholar 

  • Chen Y Y, Weaver C A, Mendelsohn D R& Burne R A (1998) Transcriptional regulation of the Streptococcus salivarius 57.I urease operon. J. Bacteriol. 180: 5769–5775.

    Google Scholar 

  • Condon S (1987) Responses of lactic acid bacteria to oxygen. FEMS Microbiol. Rev. 46: 269–280.

    Google Scholar 

  • Chen Y Y, Weaver C A& Burne R A (2000) Dual functions of Streptococcus salivarius urease. J. Bacteriol. 182: 4667–4669.

    Google Scholar 

  • Crosse A M, Greenway D L& England R R (2000) Accumulation of ppGpp and ppGp in Staphylococcus aureus 8325-4 following nutrient starvation. Lett. Appl. Microbiol. 31: 332–337.

    Google Scholar 

  • Crow V L& Thomas T D (1982) Arginine metabolism in lactic Streptococci. J. Bacteriol. 150: 1024–1032.

    Google Scholar 

  • Csonka L N& Hanson A D (1991) Prokaryotic osmoregulation: genetics and physiology. Annu. Rev. Microbiol. 45: 569–606.

    Google Scholar 

  • Cunin R, Glansdorff N, Pierard A& Stalon V (1986) Biosynthesis and metabolism of arginine in bacteria. Microbiol. Rev. 50: 314–352.

    Google Scholar 

  • Cvitkovitch D G, Gutierrez J A, Behari J, Youngman P J, Wetz J E, Crowley P F, Hillman J D, Brady L J& Bleiweis A S (2000) Tn917-lac mutagenesis of Streptococcus mutans to identify environmentally regulated genes. FEMS Microbiol. Lett. 182: 149–154.

    Google Scholar 

  • De Angelis M, Bini L, Pallini V, Cocconcelli P S& Gobbetti M (2001) The acid-stress response in Lactobacillus sanfranciscensis CB1. Microbiology 147: 1863–1873.

    Google Scholar 

  • de Urraza P& de Antoni G (1997) Induced cryotolerance of Lactobacillus delbrueckii subsp. bulgaricus LBB by preincubation at suboptimal temperature with a fermentable sugar. Cryobiology 35: 159–164.

    Google Scholar 

  • Delcour J, Ferain T, Deghorain M, Palumbo E& Hols P (1999) The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie Van Leeuwenhoek 76: 159–184.

    Google Scholar 

  • Delmas F, Pierre F, Coucheney F, Divies C& Guzzo J (2001) Biochemical and physiological studies of the small heat shock protein Lo18 from the lactic acid bacterium Oenococcus oeni. J. Mol. Microbiol. Biotechnol. 3: 601–610.

    Google Scholar 

  • Derre 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: 117–131.

    Google Scholar 

  • Derzelle S, Hallet B, Francis K P, Ferain T, Delcour J& Hols P (2000) Changes in cspL, cspP, and cspC mRNA abundance as a function of cold shock and growth phase in Lactobacillus plantarum. J. Bacteriol. 182: 5105–5113.

    Google Scholar 

  • Diaz-Torres M L& Russell R R (2001) HtrA protease and processing of extracellular proteins of Streptococcus mutans. FEMS Microbiol. Lett. 204: 23–28.

    Google Scholar 

  • Drici-Cachon Z, Guzzo J, Cavin J-F& Diviès C (1996) Acid tolerance in Leuconostoc oenos. Isolation and characterization of an acid-resistant mutant. Appl. Microbiol. Biotechnol. 44: 785–789.

    Google Scholar 

  • Dunne C, Murphy L, Flynn S, O'Mahony L, O'Halloran S, Feeney M, Morrissey D, Thornton G, Fitzgerald G, Daly C, Kiely B, Quigley E M, O'Sullivan G C, Shanahan F& Collins J K (1999) Probiotics: from myth to reality. Demonstration of functionality in animal models of disease and in human clinical trials. Antonie Van Leeuwenhoek 76: 279–292.

    Google Scholar 

  • Duwat P, Ehrlich S D& Gruss A (1995) The recA gene of Lactococcus lactis: characterization and involvement in oxidative and thermal stress. Mol. Microbiol. 17: 1121–1131.

    Google Scholar 

  • Duwat P, Ehrlich S D& Gruss A (1999) Effects of metabolic flux on stress response pathways in Lactococcus lactis. Mol. Microbiol. 31: 845–858.

    Google Scholar 

  • Duwat P, Sourice S, Cesselin B, Lamberet G, Vido K, Gaudu P, Le Loir Y, Violet F, Loubiere P& Gruss A (2001) Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival. J. Bacteriol. 183: 4509–4516.

    Google Scholar 

  • Earnshaw R G, Appleyard J& Hurst R M (1995) Understanding physical inactivation processes: combined preservation opportunities using heat, ultrasound and pressure. Int. J. Food Microbiol. 28: 197–219.

    Google Scholar 

  • Eaton T, Shearman C& Gasson M (1993) Cloning and sequence analysis of the dnaK gene region of Lactococcus lactis subsp. lactis. J. Gen. Microbiol. 139: 3253–3264.

    Google Scholar 

  • Elkins C A& Savage D C (1998) Identification of genes encoding conjugated bile salt hydrolase and transport in Lactobacillus johnsonii 100-100. J. Bacteriol. 180: 4344–4349.

    Google Scholar 

  • Engesser D M& Hammes W P (1994) Non-heme catalase activity of lactic acid bacteria. Syst. Appl. Microbiol. 17: 11–19.

    Google Scholar 

  • Eymann C, Mach H, Harwood C R& Hecker M (1996) Phosphate-starvation-inducible proteins in Bacillus subtilis: a two-dimensional gel electrophoresis study. Microbiology 142: 3163–3170.

    Google Scholar 

  • Fabret C& Hoch J A (1998) A two-component signal transduction system essential for growth of Bacillus subtilis: implications for anti-infective therapy. J. Bacteriol. 180: 6375–6383.

    Google Scholar 

  • Fang L, Jiang W, Bae W& Inouye M (1997) Promoter-independent cold-shock induction of cspA and its derepression at 37 degrees C by mRNA stabilization. Mol. Microbiol. 23: 355–364.

    Google Scholar 

  • Fenoll A, Munoz R, Garcia E& de la Campa A G (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.

    Google Scholar 

  • Ferretti J. J, McShan W M, Ajdic D, Savic D J, Savic G, Lyon K, Primeaux C, Sezate S, Suvorov A N, Kenton S, Lai H S, Lin S P, Qian Y, Jia H G, Najar F Z, Ren Q, Zhu H, Song L, White J, Yuan X, Clifton S W, Roe B A& McLaughlin R (2001) Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc. Natl. Acad. Sci. U.S.A. 98: 4658–4663.

    Google Scholar 

  • Fitzgerald J R& Musser J M (2001) Evolutionary genomics of pathogenic bacteria. Trends Microbiol. 9: 547–553.

    Google Scholar 

  • Flahaut S, Frere J, Boutibonnes P& Auffray Y (1996a) Comparison of the bile salts and sodium dodecyl sulfate stress responses in Enterococcus faecalis. Appl. Environ. Microbiol. 62: 2416–2420.

    Google Scholar 

  • Flahaut S, Hartke A, Giard J C, Benachour A, Boutibonnes P& Auffray Y (1996b) Relationship between stress response toward bile salts, acid and heat treatment in Enterococcus faecalis. FEMS Microbiol. Lett. 138: 49–54.

    Google Scholar 

  • Foucaud-Sceunemann C&Poquet I (2002) The Lactococcus lactis HtrA protease is induced and essential for cell survival under stress conditions. In preparation.

  • Francis K P, Mayr R, von Stetten F, Stewart G S& Scherer S (1998) Discrimination of psychrotrophic and mesophilic strains of the Bacillus cereus group by PCR targeting of major cold shock protein genes. Appl. Environ. Microbiol. 64: 3525–3529.

    Google Scholar 

  • Frees D& Ingmer H (1999) ClpP participates in the degradation of misfolded protein in Lactococcus lactis. Mol. Microbiol. 31: 79–87.

    Google Scholar 

  • Frees D, Varmanen P& Ingmer H (2001) Inactivation of a gene that is highly conserved in Gram-positive bacteria stimulates degradation of non-native proteins and concomitantly increases stress tolerance in Lactococcus lactis. Mol. Microbiol. 41: 93–103.

    Google Scholar 

  • Futai M, Noumi T& Maeda M (1989) ATP synthase (H+-ATPase): results by combined biochemical and molecular biological approaches. Annu. Rev. Biochem. 58: 111–136.

    Google Scholar 

  • Galperin M Y, Walker D R& Koonin E V (1998) Analogous enzymes: independent inventions in enzyme evolution. Genome Res. 8: 779–790.

    Google Scholar 

  • Garcia-Quintans N, Magni C, de Mendoza D& Lopez P (1998) The citrate transport system of Lactococcus lactis subsp. lactis biovar diacetylactis is induced by acid stress. Appl. Environ. Microbiol. 64: 850–857.

    Google Scholar 

  • Giard J C, Hartke A, Flahaut S, Benachour A, Boutibonnes P& Auffray Y (1996) Starvation-induced multiresistance in Enterococcus faecalis JH2-2. Curr. Microbiol. 32: 264–271.

    Google Scholar 

  • Giard J C, Hartke A, Flahaut S, Boutibonnes P& Auffray Y (1997) Glucose starvation response in Enterococcus faecalis JH2-2: survival and protein analysis. Res. Microbiol. 148: 27–35.

    Google Scholar 

  • Giard J C, Rince A, Capiaux H, Auffray Y& Hartke A (2000) Inactivation of the stress-and starvation-inducible gls24 operon has a pleiotrophic effect on cell morphology, stress sensitivity, and gene expression in Enterococcus faecalis. J. Bacteriol. 182: 4512–4520.

    Google Scholar 

  • Giard J C, Laplace J M, Rince A, Pichereau V, Benachour A, Leboeuf C, Flahaut S, Auffray Y& Hartke A (2001) The stress proteome of Enterococcus faecalis. Electrophoresis 22: 2947–2954.

    Google Scholar 

  • Glaasker E, Konings W N& Poolman B (1996a) Glycine betaine fluxes in Lactobacillus plantarum during osmostasis and hyperand hypo-osmotic shock. J. Biol. Chem. 271: 10060–10065.

    Google Scholar 

  • Glaasker E, Konings W N& Poolman B (1996b) Osmotic regulation of intracellular solute pools in Lactobacillus plantarum. J. Bacteriol. 178: 575–582.

    Google Scholar 

  • Glaasker E, Heuberger E H, Konings W N& Poolman B (1998a) Mechanism of osmotic activation of the quaternary ammonium compound transporter (QacT) of Lactobacillus plantarum. J Bacteriol. 180: 5540–5546.

    Google Scholar 

  • Glaasker E, Tjan F S, Ter Steeg P F, Konings W N& Poolman B (1998b) Physiological response of Lactobacillus plantarum to salt and nonelectrolyte stress. J. Bacteriol. 180: 4718–4723.

    Google Scholar 

  • Goldenberg D, Azar I& Oppenheim A B (1996) Differential mRNA stability of the cspA gene in the cold-shock response of Escherichia coli. Mol. Microbiol. 19: 241–248.

    Google Scholar 

  • Gordia S& Gutierrez C (1996) Growth-phase-dependent expression of the osmotically inducible gene osmC of Escherichia coli K-12. Mol. Microbiol. 19: 729–736.

    Google Scholar 

  • Gostick D O, Griffin H G, Shearman C A, Scott C, Green J, Gasson M J& Guest J R (1999) Two operons that encode FNR-like proteins in Lactococcus lactis. Mol. Microbiol. 31: 1523–1535.

    Google Scholar 

  • Gouesbet G, Jan G& Boyaval P (2002) Two-dimensional electrophoresis study of Lactobacillus delbrueckii subsp. bulgaricus thermotolerance. Appl. Environ. Microbiol. 68: 1055–1063.

    Google Scholar 

  • Graumann P, Schroder K, Schmid R& Marahiel M A (1996) Cold shock stress-induced proteins in Bacillus subtilis. J. Bacteriol. 178: 4611–4619.

    Google Scholar 

  • Graumann P, Wendrich T M, Weber M H, Schroder K& Marahiel M A (1997) A family of cold shock proteins in Bacillus subtilis is essential for cellular growth and for efficient protein synthesis at optimal and low temperatures. Mol. Microbiol. 25: 741–756.

    Google Scholar 

  • Grkovic S, Brown M H& Skurray R A (2001) Transcriptional regulation of multidrug efflux pumps in bacteria. Semin. Cell Dev. Biol. 12: 225–237.

    Google Scholar 

  • Guedon E, Serror P, Ehrlich S D, Renault P& Delorme C (2001) Pleiotropic transcriptional repressor CodY senses the intracellular pool of branched-chain amino acids in Lactococcus lactis. Mol. Microbiol. 40: 1227–1239.

    Google Scholar 

  • Guerzoni M E, Lanciotti R& Cocconcelli P S (2001) Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. Microbiology 147: 2255-2264.

    Google Scholar 

  • Guillot A, Obis D& Mistou M Y (2000) Fatty acid membrane composition and activation of glycine-betaine transport in Lactococcus lactis subjected to osmotic stress. Int. J. Food Microbiol. 55: 47–51.

    Google Scholar 

  • Gunn J S (2000) Mechanisms of bacterial resistance and response to bile. Microbes Infect. 2: 907–913.

    Google Scholar 

  • Gutierrez J A, Crowley P J, Brown D P, Hillman J D, Youngman P& Bleiweis A S (1996) Insertional mutagenesis and recovery of interrupted genes of Streptococcus mutans by using transposon Tn917: preliminary characterization of mutants displaying acid sensitivity and nutritional requirements. J. Bacteriol. 178: 4166–4175.

    Google Scholar 

  • Gutierrez J A, Crowley P J, Cvitkovitch D G, Brady L J, Hamilton I R, Hillman J D& Bleiweis A S (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: 357–366.

    Google Scholar 

  • Guzzo J, Cavin J& Divies C (1994) Induction of stress proteins in Leuconostoc oenos to perform direct inoculation of wine. Biotechnol. Lett. 16: 1189–1194.

    Google Scholar 

  • Guzzo J, Delmas F, Pierre F, Jobin M P, Samyn B, Van Beeumen J, Cavin J F& Divies C (1997) A small heat shock protein from Leuconostoc oenos induced by multiple stresses and during stationary growth phase. Lett. Appl. Microbiol. 24: 393–396.

    Google Scholar 

  • Guzzo J, Jobin M-P, Delmas F, Fortier L-C, 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.

    Google Scholar 

  • Hahn K, Faustoferri R C& Quivey Jr. R G (1999) Induction of an AP endonuclease activity in Streptococcus mutans during growth at low pH. Mol. Microbiol. 31: 1489–1498.

    Google Scholar 

  • Hanna M M& Liu K (1998) Nascent RNA in transcription complexes interacts with CspE, a small protein in E. coli implicated in chromatin condensation. J. Mol. Biol. 282: 227–239.

    Google Scholar 

  • Hanna M N, Ferguson R J, Li Y H& Cvitkovitch D G (2001) uvrA is an acid-inducible gene involved in the adaptive response to low pH in Streptococcus mutans. J. Bacteriol. 183: 5964–5973.

    Google Scholar 

  • Hansen M C, Nielsen A K, Molin S, Hammer K, Kilstrup M, Palmer Jr. R J, Udsen C& White D C (2001) Changes in rRNA levels during stress invalidates results from mRNA blotting: fluorescence in situ rRNA hybridization permits renormalization for estimation of cellular mRNA levels. J. Bacteriol. 183: 4747–4751.

    Google Scholar 

  • Harper D S& Loesche W J (1984) Growth and acid tolerance of human dental plaque bacteria. Arch. Oral Biol. 29: 843–848.

    Google Scholar 

  • Hartke A, Bouché S, Gansel X, Boutibonnes P& Auffray Y (1994) Starvation-induced stress resistance in Lactococcus lactis subsp. lactis IL1403. Appl. Environ. Microbiol. 60: 3474–3478.

    Google Scholar 

  • Hartke A, Bouche S, Laplace J-M, Benachour A, Boutibonnes P& Auffray Y (1995) UV-inducible proteins and UV-induced crossprotection against acid, ethanol, H2O2 or heat treatments in Lactococcus lactis subsp. lactis. Arch. Microbiol. 163: 329–336.

    Google Scholar 

  • Hartke A, Bouché S, Giard J C, Benachour A, Boutibonnes P& Auffray Y (1996) The lactic acid stress response of Lactococcus lactis subsp. lactis. Curr. Microbiol. 33: 194–199.

    Google Scholar 

  • Hartke A, Frere J, Boutibonnes P& Auffray Y (1997) Differential induction of the chaperonin GroEL and the Co-chaperonin GroES by heat, acid, and UV-irradiation in Lactococcus lactis subsp. lactis. Curr. Microbiol. 34: 23–26.

    Google Scholar 

  • Hartke A, Giard J C, Laplace J M& Auffray Y (1998) Survival of Enterococcus faecalis in an oligotrophic microcosm: changes inmorphology, development of general stress resistance, and analysis of protein synthesis. Appl. Environ. Microbiol. 64: 4238–4245.

    Google Scholar 

  • Hengge-Aronis R (1993) Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli. Cell 72: 165–168.

    Google Scholar 

  • Hengge-Aronis R (1999) Interplay of global regulators and cell physiology in the general stress response of Escherichia coli. Curr. Opin. Microbiol. 2: 148–152.

    Google Scholar 

  • Hertel C, Schmidt G, Fischer M, Oellers K& Hammes W P (1998) Oxygen-dependent regulation of the expression of the catalase gene katA of Lactobacillus sakei LTH677. Appl. Environ. Microbiol. 64: 1359–1365.

    Google Scholar 

  • Higgins C F (1992) ABC transporters: from microorganisms toman. Annu. Rev. Cell Biol. 8: 67–113.

    Google Scholar 

  • Higuchi T, Hayashi H& Abe K (1997) Exchange of glutamate and gamma-aminobutyrate in a Lactobacillus strain. J. Bacteriol. 179: 3362–3364.

    Google Scholar 

  • Hoskins J, Alborn Jr. W E, Arnold J, Blaszczak L C, Burgett S, DeHoff B S, Estrem S T, Fritz L, Fu D J, Fuller W, Geringer C, Gilmour R, Glass J S, Khoja H, Kraft A R, Lagace R E, LeBlanc D J, Lee L N, Lefkowitz E J, Lu J, Matsushima P, McAhren S M, McHenney M, McLeaster K, Mundy C W, Nicas T I, Norris F H, O'Gara M, Peery R B, Robertson G T, Rockey P, Sun P M, Winkler M E, Yang Y, Young-Bellido M, Zhao G, Zook C A, Baltz R H, Jaskunas S R, Rosteck Jr. P R, Skatrud P L& Glass J I (2001) Genome of the bacterium Streptococcus pneumoniae strain R6. J. Bacteriol. 183: 5709–5717.

    Google Scholar 

  • Hutkins R W& Nannen N L (1993) pH homeostasis in lactic acid bacteria. J. Dairy Sci. 76: 2354–2365.

    Google Scholar 

  • Hutkins R W, Ellefson W L& Kashket E R (1987) Betaine transport imparts osmotolerance on a strain of Lactobacillus acidophilus. Appl. Environ. Microbiol. 53: 2275–2281.

    Google Scholar 

  • Igarashi T, Kono Y& Tanaka K (1996) Molecular cloning of manganese catalase from Lactobacillus plantarum. J. Biol. Chem. 271: 29521–29524.

    Google Scholar 

  • Ingmer H, Vogensen F K, Hammer K& Kilstrup M (1999) Disruption and analysis of the clpB, clpC, and clpE genes in Lactococcus lactis: ClpE, a new Clp family in gram-positive bacteria. J. Bacteriol. 181: 2075–2083.

    Google Scholar 

  • Irvine A S& Guest J R (1993) Lactobacillus casei contains a member of the CRP-FNR family. Nucleic Acids Res. 21: 753.

    Google Scholar 

  • Israelsen H, Madsen S M, Vrang A, Hansen E B& Johansen E (1995) Cloning and partial characterization of regulated promoters from Lactococcus lactis Tn917-lacZ integrants with the new promoter probe vector, pAK80. Appl. Environ. Microbiol. 61: 2540–2547.

    Google Scholar 

  • Jayaraman G C, Penders J E& Burne R A (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.

    Google Scholar 

  • Jensen N B, Melchiorsen C R, Jokumsen K V& Villadsen J (2001) Metabolic behavior of Lactococcus lactis MG1363 in microaerobic continuous cultivation at a low dilution rate. Appl. Environ. Microbiol. 67: 2677–2682.

    Google Scholar 

  • Jiang W, Fang L& Inouye M (1996) The role of the 5'-end untranslated region of the mRNA for CspA, the major cold-shock protein of Escherichia coli, in cold-shock adaptation. J. Bacteriol. 178: 4919–4925.

    Google Scholar 

  • Jiang W, Hou Y& Inouye M (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 272: 196–202.

    Google Scholar 

  • Jobin M P, Garmyn D, Divies C& Guzzo J (1999) Expression of the Oenococcus oeni trxA gene is induced by hydrogen peroxide and heat shock. Microbiology 145: 1245-1251.

    Google Scholar 

  • Kaan T, Jurgen B& Schweder T (1999) Regulation of the expression of the cold shock proteins CspB and CspC in Bacillus subtilis. Mol. Gen. Genet. 262: 351–354.

    Google Scholar 

  • Kashket E R (1984) Bioenergetics of lactic acid bacteria: cytoplasmic pH and osmotolerance. FEMS Microbiol. Rev. 46: 233–244.

    Google Scholar 

  • Kashket E R& Barker S L (1977) Effects of potassium ions on the electrical and pH gradients across the membrane of Streptococcus lactis cells. J. Bacteriol. 130: 1017–1023.

    Google Scholar 

  • Kets E P W, Teunissen P J M& De Bont J A M (1996) Effect of compatible solutes on survival of lactic acid bacteria subjected to drying. Appl. Environ. Microbiol. 62: 259–261.

    Google Scholar 

  • Kilstrup M, Jacobsen S, Hammer K& Vogensen F K (1997) Induction of heat shock proteins DnaK, GroEL, and GroES by salt stress in Lactococcus lactis. Appl. Environ. Microbiol. 63: 1826–1837.

    Google Scholar 

  • Kim S G& Batt C A (1993) Cloning and sequencing of the Lactococcus lactis subsp. lactis groESL operon. Gene. 127: 121–126.

    Google Scholar 

  • Kim W S& Dunn N W (1997) Identification of a cold shock gene in lactic acid bacteria and the effect of cold shock on cryotolerance. Curr. Microbiol. 35: 59–63.

    Google Scholar 

  • Kim W S, Khunajakr N& Dunn N W (1998) Effect of cold shock on protein synthesis and on cryotolerance of cells frozen for long periods in Lactococcus lactis. Cryobiology 37: 86–91.

    Google Scholar 

  • Kim W S, Ren J& Dunn N W (1999) Differentiation of Lactococcus lactis subspecies lactis and subspecies cremoris strains by their adaptive response to stresses. FEMS Microbiol. Lett. 171: 57–65.

    Google Scholar 

  • Kim W S, Perl L, Park J H, Tandianus J E& Dunn N W (2001) Assessment of stress response of the probiotic Lactobacillus acidophilus. Curr. Microbiol. 43: 346–350.

    Google Scholar 

  • Knauf H J, Vogel R F& Hammes W P (1992) Cloning, sequence, and phenotypic expression of katA, which encodes the catalase of Lactobacillus sake LTH677. Appl. Environ. Microbiol. 58: 832–839.

    Google Scholar 

  • Kobayashi H, Murakami N& Unemoto T (1982) Regulation of the cytoplasmic pH in Streptococcus faecalis. J. Biol. Chem. 257: 13246–13252.

    Google Scholar 

  • Koch B, Kilstrup M, Vogensen F K& Hammer K (1998) Induced levels of heat shock proteins in a dnaK mutant of Lactococcus lactis. J. Bacteriol. 180: 3873–3881.

    Google Scholar 

  • Koebmann B J, Nilsson D, Kuipers O P& Jensen P R (2000) The membrane-bound H(+)-ATPase complex is essential for growth of Lactococcus lactis. J. Bacteriol. 182: 4738–4743.

    Google Scholar 

  • Komatsu Y, Kaul S C, Iwahashi H& Obuchi K (1990) Do heat shock proteins provide protection against freezing? FEMS Microbiol. Lett. 60: 159–162.

    Google Scholar 

  • Konings W N, Lolkema J S, Bolhuis H, van Veen H W, Poolman B& Driessen A J (1997) The role of transport processes in survival of lactic acid bacteria. Energy transduction and multidrug resistance. Antonie Van Leeuwenhoek. 71: 117–128.

    Google Scholar 

  • Kono Y& Fridovich I (1983) Isolation and characterization of the pseudocatalase of Lactobacillus plantarum. J. Biol. Chem. 258: 6015–6019.

    Google Scholar 

  • Koonin E V, Aravind L& Glaperin M Y (2000) A comparativegenomic view of the microbial stress response. In: Stortz G& Hengge-Aronis R (Eds.) Bacterial Stress Responses (pp 417–444). ASM Press, Washington, DC.

    Google Scholar 

  • Kornberg A, Rao N N& Ault-Riche D (1999) Inorganic polyphosphate: a molecule of many functions. Annu. Rev. Biochem. 68: 89–125.

    Google Scholar 

  • Kremer B H, van der Kraan M, Crowley P J, Hamilton I R, Brady L J& Bleiweis A S (2001) Characterization of the sat operon in Streptococcus mutans: evidence for a role of Ffh in acid tolerance. J. Bacteriol. 183: 2543–2552.

    Google Scholar 

  • Kullen M J& Klaenhammer T R (1999) Identification of the pHinducible, proton-translocating F1F0-ATPase (atpBEFHAGDC) operon of Lactobacillus acidophilus by differential display: gene structure, cloning and characterization. Mol. Microbiol. 33: 1152–1161.

    Google Scholar 

  • Kunji E R, Ubbink T, Matin A, Poolman B& Konings W N (1993) Physiological responses of Lactococcus lactis ML3 to alternating conditions of growth and starvation. Arch. Microbiol. 159: 372–379.

    Google Scholar 

  • Kuroda A, Nomura K, Ohtomo R, Kato J, Ikeda T, Takiguchi N, Ohtake H& Kornberg A (2001) Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science 293: 705–708.

    Google Scholar 

  • Kvint K, Farewell A& Nystrom T (2000) RpoS-dependent promoters require guanosine tetraphosphate for induction even in the presence of high levels of sigma(s). J. Biol. Chem. 275: 14795–14798.

    Google Scholar 

  • Lange R& Hengge-Aronis R (1991) Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S. J. Bacteriol. 173: 4474–4481.

    Google Scholar 

  • Laport M S, de Castro A C, Villardo A, Lemos J A, Bastos M C& Giambiagi-deMarval M (2001) Expression of the major heat shock proteins DnaK and GroEL in Streptococcus pyogenes: a comparison to Enterococcus faecalis and Staphylococcus aureus. Curr. Microbiol. 42: 264–268.

    Google Scholar 

  • Lawrence J G, Hendrix R W& Casjens S (2001) Where are the pseudogenes in bacterial genomes? Trends Microbiol. 9: 535–540.

    Google Scholar 

  • Lemos J A, Chen Y Y& Burne R A (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: 6074–6084.

    Google Scholar 

  • Li Y H, Hanna M N, Svensater G, Ellen R P& Cvitkovitch D G (2001) Cell density modulates acid adaptation in Streptococcus mutans: implications for survival in biofilms. J. Bacteriol. 183: 6875–6884.

    Google Scholar 

  • Lim E M, Ehrlich S D& Maguin E (2000) Identification of stress-inducible proteins in Lactobacillus delbrueckii subsp. bulgaricus. Electrophoresis 21: 2557–2561.

    Google Scholar 

  • Lin M Y& Yen C L (1999) Antioxidative ability of lactic acid bacteria. J. Agric. Food Chem. 47: 1460–1466.

    Google Scholar 

  • Lindahl T& Nyberg B (1972) Rate of depurination of native deoxyribonucleic acid. Biochemistry 11: 3610–3618.

    Google Scholar 

  • Liu S, Asmundson R V, Gopal P K, Holland R& Crow V L (1998) Influence of reduced water activity on lactose metabolism by lactococcus lactis subsp. cremoris at different pH values. Appl. Environ. Microbiol. 64: 2111–2116.

    Google Scholar 

  • Loewen P C, Hu B, Strutinsky J& Sparling R (1998) Regulation in the rpoS regulon of Escherichia coli. Can. J. Microbiol. 44: 707–717.

    Google Scholar 

  • Lomovskaya O& Lewis K (1992) Emr, an Escherichia coli locus for multidrug resistance. Proc. Natl. Acad. Sci. U.S.A. 89: 8938–8942.

    Google Scholar 

  • Lopez de Felipe F, Kleerebezem M, de Vos W M& Hugenholtz J (1998) Cofactor engineering: a novel approach to metabolic engineering in Lactococcus lactis by controlled expression of NADH oxidase. J. Bacteriol. 180: 3804–3808.

    Google Scholar 

  • Lorca G L& de Valdez G F (1999) The effect of suboptimal growth temperature and growth phase on resistance of Lactobacillus acidophilus to environmental stress. Cryobiology 39: 144–149.

    Google Scholar 

  • Lorca G L& Valdez G F (2001) A low-pH-inducible, stationaryphase acid tolerance response in Lactobacillus acidophilus CRL 639. Curr. Microbiol. 42: 21–25.

    Google Scholar 

  • Ma Y& Marquis R E (1997) Thermophysiology of Streptococcus mutans and related lactic-acid bacteria. Antonie Van Leeuwenhoek 72: 91–100.

    Google Scholar 

  • Ma D, Cook D N, Hearst J E& Nikaido H (1994) Efflux pumps and drug resistance in gram-negative bacteria. Trends Microbiol. 2: 489–493.

    Google Scholar 

  • Ma Y, Curran T M& Marquis R E (1997) Rapid procedure for acid adaptation of oral lactic-acid bacteria and further characterization of the response. Can. J. Microbiol. 43: 143–148.

    Google Scholar 

  • Mallonee D H& Hylemon P B (1996) Sequencing and expression of a gene encoding a bile acid transporter from Eubacterium sp. strain VPI 12708. J. Bacteriol. 178: 7053–7058.

    Google Scholar 

  • Markham P N& Neyfakh A A (2001) Efflux-mediated drug resistance in Gram-positive bacteria. Curr. Opin. Microbiol. 4: 509–514.

    Google Scholar 

  • Marquis R E, Bender G R, Murray D R& Wong A (1987) Arginine deiminase system and bacterial adaptation to acid environments. Appl. Environ. Microbiol. 53: 198–200.

    Google Scholar 

  • Martin-Galiano A J, Ferrandiz M J& de la Campa A G (2001) The promoter of the operon encoding the F0F1 ATPase of Streptococcus pneumoniae is inducible by pH. Mol. Microbiol. 41: 1327–1338.

    Google Scholar 

  • 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: 177–182.

    Google Scholar 

  • Marty-Teysset C, Posthuma C, Lolkema J S, Schmitt P, Divies C& Konings W N (1996) Proton motive force generation by citrolactic fermentation in Leuconostoc mesenteroides. J. Bacteriol. 178: 2178–2185.

    Google Scholar 

  • Marty-Teysset C, de la Torre F& Garel J (2000) Increased production of hydrogen peroxide by Lactobacillus delbrueckii subsp. bulgaricus upon aeration: involvement of an NADH oxidase in oxidative stress. Appl. Environ. Microbiol. 66: 262–267.

    Google Scholar 

  • Mascarenhas J, Weber M H& Graumann P L (2001) Specific polar localization of ribosomes in Bacillus subtilis depends on active transcription. EMBO Rep. 2: 685–689.

    Google Scholar 

  • Mayo B, Derzelle S, Fernandez M, Leonard C, Ferain T, Hols P, Suarez J E& Delcour J (1997) Cloning and characterization of cspL and cspP, two cold-inducible genes from Lactobacillus plantarum. J. Bacteriol. 179: 3039–3042.

    Google Scholar 

  • Mechold U, Cashel M, Steiner K, Gentry D& Malke H (1996) Functional analysis of a relA/spoT gene homolog from Streptococcus equisimilis. J. Bacteriol. 178: 1401–1411.

    Google Scholar 

  • Mercenier A, Muller-Alouf H& Grangette C (2000) Lactic acid bacteria as live vaccines. Curr. Issues Mol. Biol. 2: 17–25.

    Google Scholar 

  • Miyoshi A, Gratadoux J J, Azevedo V, Rochat T, Duwat P, Sourice S, Oliveira S C, Gruss A&Langella P (2002) Expression of heterologous catalases confers high-level resistance to oxidative stress in Lactococcus lactis. In preparation.

  • Mogk A, Homuth G, Scholz C, Kim L, Schmid F X& Schumann W(1997) The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. EMBO J. 16: 4579–4590.

    Google Scholar 

  • Molenaar D, Bosscher J S, ten Brink B, Driessen A J& Konings W N (1993) Generation of a proton motive force by histidine decarboxylation and electrogenic histidine/histamine antiport in Lactobacillus buchneri. J. Bacteriol. 175: 2864–2870.

    Google Scholar 

  • Moser S A& Savage D C (2001) Bile salt hydrolase activity and resistance to toxicity of conjugated bile salts are unrelated properties in lactobacilli. Appl. Environ. Microbiol. 67: 3476–3480.

    Google Scholar 

  • Nannen N L& Hutkins R W (1991) Proton translocating adenosine triphosphatase activity in lacic acid bacteria. J. Dairy Sci. 74: 747–751.

    Google Scholar 

  • Nilsson D, Lauridsen A A, Tomoyasu T& Ogura T (1994) A Lactococcus lactis gene encodes a membrane protein with putative ATPase activity that is homologous to the essential Escherichia coli ftsH gene product. Microbiology 140: 2601–2610.

    Google Scholar 

  • Nishino K& Yamaguchi A (2001) Analysis of a complete library of putative drug transporter genes in Escherichia coli. J. Bacteriol. 183: 5803–5812.

    Google Scholar 

  • Obis D, Guillot A, Gripon J C, Renault P, Bolotin A& Mistou M Y (1999) Genetic and biochemical characterization of a high-affinity betaine uptake system (BusA) in Lactococcus lactis reveals a new functional organization within bacterial ABC transporters. J. Bacteriol. 181: 6238–6246.

    Google Scholar 

  • O'Connell-Motherway M, van Sinderen D, Morel-Deville F, Fitzgerald G F, Ehrlich S D& Morel P (2000) Six putative twocomponent regulatory systems isolated from Lactococcus lactis subsp. cremoris MG1363. Microbiology 146: 935–947.

    Google Scholar 

  • Olsen E B, Russell J B& Henick-Kling T (1991) Electrogenic L-malate transport by Lactobacillus plantarum: a basis for energy derivation from malolactic fermentation. J. Bacteriol. 173: 6199–6206.

    Google Scholar 

  • 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: 2287–2293.

    Google Scholar 

  • Panoff J M, Legrand S, Thammavongs B& Boutibonnes P (1994) The cold shock response in Lactococcus subsp. lactis. Curr. Microbiol. 29: 213–216.

    Google Scholar 

  • 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: 516–520.

    Google Scholar 

  • Panoff J M, Corroler D, Thammavongs B& Boutibonnes P (1997) Differentiation between cold shock proteins and cold acclimation proteins in a mesophilic gram-positive bacterium, Enterococcus faecalis JH2-2. J. Bacteriol. 179: 4451–4454.

    Google Scholar 

  • Panoff J M, Thammavongs B& Gueguen M (2000) Cryoprotectants lead to phenotypic adaptation to freeze-thaw stress in Lactobacillus delbrueckii ssp. bulgaricus CIP 101027T. Cryobiology 40: 264–269.

    Google Scholar 

  • Pebay M, Holl A C, Simonet J M& Decaris B (1995) Characterization of the gor gene of the lactic acid bacterium Streptococcus thermophilus CNRZ368. Res. Microbiol. 146: 371–383.

    Google Scholar 

  • Perrin C, Guimont C, Bracquart P& Gaillard J L (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: 342–347.

    Google Scholar 

  • Persuh M, Turgay K, Mandic-Mulec I& Dubnau D (1999) The Nand C-terminal domains of MecA recognize different partners in the competence molecular switch. Mol. Microbiol. 33: 886–894.

    Google Scholar 

  • Petersohn A, Brigulla M, Haas S, Hoheisel J D, Volker U& Hecker M (2001) Global analysis of the general stress response of Bacillus subtilis. J. Bacteriol. 183: 5617–5631.

    Google Scholar 

  • Phadtare S& Inouye M(1999) Sequence-selective interactions with RNA by CspB, CspC and CspE, members of the CspA family of Escherichia coli. Mol. Microbiol. 33: 1004–1014.

    Google Scholar 

  • Phadtare S, Yamanata K& Inouye M (2000) The cold-shock response. In: Stortz G& Hengge-Aronis R (Eds.) Bacterial Stress Response (pp 33–45). ASM Press, Washington, DC.

    Google Scholar 

  • Poolman B, Nijssen R M& Konings W N (1987a) Dependence of Streptococcus lactis phosphate transport on internal phosphate concentration and internal pH. J. Bacteriol. 169: 5373–5378.

    Google Scholar 

  • Poolman B, Smid E J, Veldkamp H& Konings W (1987b) Bioenergetic consequences of lactose starvation for continuously cultured Streptococcus cremoris and Streptococcus lactis. J. Bacteriol. 169: 1460–1468.

    Google Scholar 

  • Poolman B, Molenaar D, Smid E J, Ubbink T, Abee T, Renault P P& Konings W N (1991) Malolactic fermentation: electrogenic malate uptake and malate/lactate antiport generate metabolic energy. J. Bacteriol. 173: 6030–6037.

    Google Scholar 

  • Poolman B& Glaasker E (1998) Regulation of compatible solute accumulation in bacteria. Mol. Microbiol. 29: 397–407.

    Google Scholar 

  • Poquet I, Saint V, Seznec E, Simoes N, Bolotin A& Gruss A (2000) HtrA is the unique surface housekeeping protease in Lactococcus lactis and is required for natural protein processing. Mol. Microbiol. 35: 1042–1051.

    Google Scholar 

  • Presser K A, Ratkowsky D A& Ross T (1997) Modelling the growth rate of Escherichia coli as a function of pH and lactic acid concentration. Appl. Environ. Microbiol. 63: 2355–2360.

    Google Scholar 

  • Price C W, Fawcett P, Ceremonie H, Su N, Murphy C K& Youngman P (2001) Genome-wide analysis of the general stress response in Bacillus subtilis. Mol. Microbiol. 41: 757–774.

    Google Scholar 

  • Prieto-Alamo M J, Jurado J, Gallardo-Madueno R, Monje-Casas F, Holmgren A& Pueyo C (2000) Transcriptional regulation of glutaredoxin and thioredoxin pathways and related enzymes in response to oxidative stress. J. Biol. Chem. 275: 13398–13405.

    Google Scholar 

  • Provenzano D& Klose K E (2000) Altered expression of the ToxR-regulated porins OmpU and OmpT diminishes Vibrio cholerae bile resistance, virulence factor expression, and intestinal colonization. Proc. Natl. Acad. Sci. U.S.A. 97: 10220–10224.

    Google Scholar 

  • Putman M, van Veen H W& Konings W N (2000) Molecular properties of bacterial multidrug transporters. Microbiol. Mol. Biol. Rev. 64: 672–693.

    Google Scholar 

  • Quivey Jr. R G, Faustoferri R C, Clancy K A& Marquis R E (1995) Acid adaptation in Streptococcus mutans UA159 alleviates sensitization to environmental stress due to RecA deficiency. FEMS Microbiol. Lett. 126: 257–261.

    Google Scholar 

  • Quivey Jr. R G, Faustoferri R, Monahan K& Marquis R (2000a) Shifts in membrane fatty acid profiles associated with acid adaptation of Streptococcus mutans. FEMS Microbiol. Lett. 189: 89–92.

    Google Scholar 

  • Quivey Jr. R G, Kuhnert W L& Hahn K (2000b) Adaptation of oral streptococci to low pH. Adv. Microb. Physiol. 42: 239–274.

    Google Scholar 

  • Quivey R G, Kuhnert W L& Hahn K (2001) Genetics of acid adaptation in oral streptococci. Crit. Rev. Oral Biol. Med. 12: 301–314.

    Google Scholar 

  • Rallu F, Gruss A& Maguin E (1996) Lactococcus lactis and stress. Antonie van Leeuwenhoek 70: 243–251.

    Google Scholar 

  • Rallu F, Gruss A, Ehrlich S D& Maguin E (2000) Acid-and multistress-resistant mutants of Lactococcus lactis: identification of intracellular stress signals. Mol. Microbiol. 35: 517–528.

    Google Scholar 

  • Rao N N& Kornberg A (1999) Inorganic polyphosphate regulates responses of Escherichia coli to nutritional stringencies, environmental stresses and survival in the stationary phase. Prog. Mol. Subcell. Biol. 23: 183–195.

    Google Scholar 

  • Rastogi V K& Girvin M E (1999) Structural changes linked to proton translocation by subunit c of the ATP synthase. Nature 402: 263–268.

  • Renault P, Gaillardin C& Heslot H (1988) Role of malolactic fermentation in lactic acid bacteria. Biochimie 70: 375–379.

    Google Scholar 

  • Rince A, Flahaut S& Auffray Y (2000) Identification of general stress genes in Enterococcus faecalis. Int. J. Food Microbiol. 55: 87–91.

    Google Scholar 

  • Roméo Y, Gotierrez C&Mistou M Y (2002) Osmoregulation in Lactococcus lactis. BusR, a transcriptional repressor of the glycine betaine uptake system BusA. Submitted for publication.

  • Russell D W& Setchell K D (1992) Bile acid biosynthesis. Biochemistry 31: 4737–4749.

    Google Scholar 

  • Sakamoto K, Margolles A, van Veen H W& Konings W N (2001) Hop resistance in the beer spoilage bacterium Lactobacillus brevis is mediated by the ATP-binding cassette multidrug transporter HorA. J. Bacteriol. 183: 5371–5375.

    Google Scholar 

  • Salema M, Lolkema J S, San Romao M V& Lourero Dias M C (1996) The proton motive force generated in Leuconostoc oenos by L-malate fermentation. J. Bacteriol. 178: 3127–3132.

    Google Scholar 

  • Salotra P, Singh D K, Seal K P, Krishna N, Jaffe H& Bhatnagar R (1995) Expression of DnaK and GroEL homologs in Leuconostoc esenteroides in response to heat shock, cold shock or chemical stress. FEMS Microbiol. Lett. 131: 57–62.

    Google Scholar 

  • Sambongi Y, Iko Y, Tanabe M, Omote H, Iwamoto-Kihara A, Ueda I, Yanagida T, Wada Y& Futai M (1999) Mechanical rotation of the c subunit oligomer in ATP synthase (F0F1): direct observation. Science 286: 1722–1724.

    Google Scholar 

  • Sami M, Yamashita H, Hirono T, Kadokura H, Kitamoto K, Yoda K& Yamasaki M (1997) Hop-resistant Lactobacillus brevis contains a novel plasmid harboring a multidrug resistance-like gene. J. Ferment. Bioeng. 84: 1–6.

    Google Scholar 

  • Sancar A (1996) DNA excision repair. Annu. Rev. Biochem. 65: 43–81.

    Google Scholar 

  • Sanders J W, Leenhouts K J, Haandrikman A J, Venema G& Kok J (1995) Stress response in Lactococcus lactis: cloning, expression analysis, and mutation of the lactococcal superoxide dismutase gene. J. Bacteriol. 177: 5254–5260.

    Google Scholar 

  • Sanders J W, Leenhouts K, Burghoorn J, Brands J R, Venema G& Kok J (1998a) A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Mol. Microbiol. 27: 299–310.

    Google Scholar 

  • Sanders J W, Venema G, Kok J& Leenhouts K (1998b) Identification of a sodium chloride-regulated promoter in Lactococcus lactis by single-copy chromosomal fusion with a reporter gene. Mol. Gen. Genet. 257: 681–685.

    Google Scholar 

  • Sanders J W, Venema G, Kok J (1999) Environmental stress responses in Lactococcus lactis. FEMS Microbiol. Rev. 23: 483–501.

    Google Scholar 

  • Schiffrin E J& Blum S (2001) Food processing: probiotic microorganisms for beneficial foods. Curr. Opin. Biotechnol. 12: 499–502.

    Google Scholar 

  • Schmidt G, Hertel C& Hammes W P (1999) Molecular characterisation of the dnaK operon of Lactobacillus sakei LTH681. Syst. Appl. Microbiol. 22: 321–328.

    Google Scholar 

  • Scott C, Guest J R& Green J (2000a) Characterization of the Lactococcus lactis transcription factor FlpA and demonstration of an in vitro switch. Mol. Microbiol. 35: 1383–1393.

    Google Scholar 

  • Scott C, Rawsthorne H, Upadhyay M, Shearman C A, Gasson M J, Guest J R& Green J (2000b) Zinc uptake, oxidative stress and the FNR-like proteins of Lactococcus lactis. FEMS Microbiol. Lett. 192: 85–89.

    Google Scholar 

  • Shibata C, Ehara T, Tomura K, Igarashi K& Kobayashi H (1992) Gene structure of Enterococcus hirae (Streptococcus faecalis) F1F0-ATPase, which functions as a regulator of cytoplasmic pH. J. Bacteriol. 174: 6117–6124.

    Google Scholar 

  • Sijpesteijn A K (1970) Induction of cytochrome formation and stimulation of oxidative dissimilation by hemin in Streptococcus lactis and Leuconostoc mesenteroides. Antonie Van Leeuwenhoek 36: 335–348.

    Google Scholar 

  • Skinner M M& Trempy J E (2001) Expression of clpX, an ATPase subunit of the Clp protease, is heat and cold shock inducible in Lactococcus lactis. J. Dairy Sci. 84: 1783–1785.

    Google Scholar 

  • Small P L& Waterman S R (1998) Acid stress, anaerobiosis and gadCB: lessons from Lactococcus lactis and Escherichia coli. Trends Microbiol. 6: 214–216.

    Google Scholar 

  • Smeds A, Varmanen P& Palva A (1998) Molecular characterization of a stress-inducible gene from Lactobacillus helveticus. J. Bacteriol. 180: 6148–6153.

    Google Scholar 

  • Smith A J, Quivey Jr. R G& Faustoferri R C (1996) Cloning and nucleotide sequence analysis of the Streptococcus mutans membrane-bound, proton-translocating ATPase operon. Gene 183: 87–96.

    Google Scholar 

  • Somero G N (1995) Proteins and temperature. Annu. Rev. Physiol. 57: 43–68.

    Google Scholar 

  • Spiess C, Beil A& Ehrmann M (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97: 339–347.

    Google Scholar 

  • Steiner K& Malke H (2000) Life in protein-rich environments: the relA-independent response of Streptococcus pyogenes to amino acid starvation. Mol. Microbiol. 38: 1004–1016.

    Google Scholar 

  • Steiner K& Malke H (2001) relA-Independent amino acid starvation response network of Streptococcus pyogenes. J. Bacteriol. 183: 7354–7364.

    Google Scholar 

  • Stewart E J, Aslund F& Beckwith J (1998) Disulfide bond formation in the Escherichia coli cytoplasm: an in vivo role reversal for the thioredoxins. EMBO J. 17: 5543–5550.

    Google Scholar 

  • Stiles M E (1996) Biopreservation by lactic acid bacteria. Antonie Van Leeuwenhoek 70: 331–345.

    Google Scholar 

  • Stock D, Leslie A G& Walker J E (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286: 1700–1705.

    Google Scholar 

  • Stortz G& Hengge-Aronis R (Eds.) (2000) Bacterial Stress Responses (p 485). ASM Press, Washington, DC.

    Google Scholar 

  • Stuart M R, Chou L S& Weimer B C (1999) Influence of carbohydrate starvation and arginine on culturability and amino acid utilization of Lactococcus lactis subsp. lactis. Appl. Environ. Microbiol. 65: 665–673.

    Google Scholar 

  • Suzuki T, Unemoto T& Kobayashi H (1988) Novel streptococcal mutants defective in the regulation of H+-ATPase biosynhesis and in F0 complex. J. Biochem. Chem. 263: 11840–11843

    Google Scholar 

  • Svensater G, Sjogreen B& Hamilton I R (2000) Multiple stress responses in Streptococcus mutans and the induction of general and stress-specific proteins. Microbiology 146: 107–117.

    Google Scholar 

  • Takahashi N& Yamada T (1999) Acid-induced acid tolerance and acidogenicity of non-mutans streptococci. Oral Microbiol. Immunol. 14: 43–48.

    Google Scholar 

  • Teixera P, Castro H, Mohacsi-Farkas C& Kirby R (1997) Identification of sites of injury in Lactobacillus bulgaricus during heat stress. J. Appl. Microbiol. 83: 219–226.

    Google Scholar 

  • ten Brink B, Otto R, Hansen U P& Konings W N (1985) Energy recycling by lactate efflux in growing and nongrowing cells of Streptococcus cremoris. J. Bacteriol. 162: 383–390.

    Google Scholar 

  • Tettelin H, Nelson K E, Paulsen I T, Eisen J A, Read T D, Peterson S, Heidelberg J, DeBoy R T, Haft D H, Dodson R J, Durkin A S, Gwinn M, Kolonay J F, Nelson W C, Peterson J D, Umayam L A, White O, Salzberg S L, Lewis M R, Radune D, Holtzapple E, Khouri H, Wolf A M, Utterback T R, Hansen C L, McDonald L A, Feldblyum T V, Angiuoli S, Dickinson T, Hickey E K, Holt I E, Loftus B J, Yang F, Smith H O, Venter J C, Dougherty B A, Morrison D A, Hollingshead S K& Fraser C M (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498–506.

    Google Scholar 

  • Thammavongs B, Corroler D, Panoff J M, Auffray Y& Boutibonnes P (1996) Physiological response of Enterococcus faecalis JH2-2 to cold shock: growth at low temperatures and freezing/thawing challenge. Lett. Appl. Microbiol. 23: 398–402.

    Google Scholar 

  • Thanassi D G, Cheng L W& Nikaido H (1997) Active efflux of bile salts by Escherichia coli. J. Bacteriol. 179: 2512–2518.

    Google Scholar 

  • 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.

    Google Scholar 

  • Tourdot-Marechal R, Fortier L C, Guzzo J, Lee B& Divies C (1999) Acid sensitivity of neomycin-resistant mutants of Oenococcus oeni: a relationship between reduction of ATPase activity and lack of malolactic activity. FEMS Microbiol. Lett. 178: 319–326.

    Google Scholar 

  • Trainor V C, Udy R K, Bremer P J& Cook G M (1999) Survival of Streptococcus pyogenes under stress and starvation. FEMS Microbiol. Lett. 176: 421–428.

    Google Scholar 

  • Turner M S, Woodberry T, Hafner L M& Giffard P M (1999) The bspA locus of Lactobacillus fermentum BR11 encodes an L-cystine uptake system. J. Bacteriol. 181: 2192–2198.

    Google Scholar 

  • Uguen P, Hamelin J, Le Pennec J P& Blanco C (1999) Influence of osmolarity and the presence of an osmoprotectant on Lactococcus lactis growth and bacteriocin production. Appl. Environ. Microbiol. 65: 291–293.

    Google Scholar 

  • van Asseldonk M, Simons A, Visser H, de Vos W M& Simons G (1993) Cloning, nucleotide sequence, and regulatory analysis of the Lactococcus lactis dnaJ gene. J. Bacteriol. 175: 1637–1644.

    Google Scholar 

  • Van de Guchte M, Ehrlich S D& Maguin E (2001) Production of growth-inhibiting factors by Lactobacillus delbrueckii. J. Appl. Microbiol. 91: 147–153.

    Google Scholar 

  • Van der Heide T& Poolman B (2000a) Glycine betaine transport in Lactococcus lactis is osmotically regulated at the level of expression and translocation activity. J. Bacteriol. 182: 203–206.

    Google Scholar 

  • Van der Heide T& Poolman B (2000b) Osmoregulated ABCtransport system of Lactococcus lactis senses water stress via changes in the physical state of the membrane. Proc. Natl. Acad. Sci. U.S.A. 97: 7102–7106.

    Google Scholar 

  • Van der Heide T, Stuart M C& Poolman B (2001) On the osmotic signal and osmosensing mechanism of an ABC transport system for glycine betaine. EMBO J. 20: 7022–7032.

    Google Scholar 

  • van Veen HW, Putman M, Margolles A, Sakamoto K& Konings W N (1999) Structure-function analysis of multidrug transporters in Lactococcus lactis. Biochim. Biophys. Acta 1461: 201–206.

    Google Scholar 

  • van Velkinburgh J C& Gunn J S (1999) PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp. Infect. Immun. 67: 1614–1622.

    Google Scholar 

  • VanBogelen R A, Greis K D, Blumenthal M, Tani T H& Matthews R (1999) Mapping regulatory networks in microbial cells. Trends Microbiol. 7: 320–328.

    Google Scholar 

  • VanBogelen R A& Neidhardt F (1990) Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 87: 5589–5593.

    Google Scholar 

  • Varmanen P, Ingmer H& Vogensen F K (2000) ctsR of Lactococcus lactis encodes a negative regulator of clp gene expression. Microbiology 146: 1447–1455.

    Google Scholar 

  • Voelker U, Voelker A, Maul B, Hecker M, Dufour A& Haldenwang W G (1995) Separate mechanisms activate sigma B of Bacillus subtilis in response to environmental and metabolic stresses. J. Bacteriol. 177: 3771–3780.

    Google Scholar 

  • Volker U, Andersen K K, Antelmann H, Devine K M& Hecker M (1998) One of two osmC homologs in Bacillus subtilis is part of the sigmaB-dependent general stress regulon. J. Bacteriol. 180: 4212–4218.

    Google Scholar 

  • Walker D C, Girgis H S& Klaenhammer T R (1999) The groESL chaperone operon of Lactobacillus johnsonii. Appl. Environ. Microbiol. 65: 3033–3041.

    Google Scholar 

  • Wang N, Yamanaka K& Inouye M (1999) CspI, the ninth member of the CspA family of Escherichia coli, is induced upon cold shock. J. Bacteriol. 181: 1603–1609.

    Google Scholar 

  • Weber M H, Beckering C L& Marahiel M A (2001a) Complementation of cold shock proteins by translation initiation factor IF1 in vivo. J. Bacteriol. 183: 7381–7386.

    Google Scholar 

  • Weber M H, Volkov A V, Fricke I, Marahiel M A& Graumann P L (2001b) Localization of cold shock proteins to cytosolic spaces surrounding nucleoids in Bacillus subtilis depends on active transcription. J. Bacteriol. 183: 6435–6443.

    Google Scholar 

  • Wehmeier L, Schafer A, Burkovski A, Kramer R, Mechold U, Malke H, Puhler A& Kalinowski J (1998) The role of the Corynebacterium glutamicum rel gene in (p)ppGpp metabolism. Microbiology 144: 1853–1862.

    Google Scholar 

  • Wells J M, Robinson K, Chamberlain L M, Schofield K M& Le Page R W (1996) Lactic acid bacteria as vaccine delivery vehicles. Antonie Van Leeuwenhoek 70: 317–330.

    Google Scholar 

  • Wendrich T M& Marahiel M A (1997) Cloning and characterization of a relA/spoT homologue from Bacillus subtilis. Mol. Microbiol. 26: 65–79.

    Google Scholar 

  • Whitaker R D& Batt C A (1991) Characterization of the heat shock response in Lactococcus lactis subsp. lactis. Appl. Environ. Microbiol. 57: 1408–1412.

    Google Scholar 

  • Whitehead K E, Webber G M& England R R (1998) Accumulation of ppGpp in Streptococcus pyogenes and Streptococcus rattus following amino acid starvation. FEMS Microbiol. Lett. 159: 21–26.

    Google Scholar 

  • Wilkins J C, Homer K A& 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.

    Google Scholar 

  • Willimsky G, Bang H, Fischer G& Marahiel M A (1992) Characterization of cspB, a Bacillus subtilis inducible cold shock gene affecting cell viability at low temperatures. J. Bacteriol. 174: 6326–6335.

    Google Scholar 

  • Wouters J A, Frenkiel H, de Vos W M, Kuipers O P& Abee T (2001) Cold shock proteins of Lactococcus lactis MG1363 are involved in cryoprotection and in the production of cold-induced proteins. Appl. Environ. Microbiol. 67: 5171–5178.

    Google Scholar 

  • Wouters J A, Sanders J W, Kok J, de Vos W M, Kuipers O P& Abee T (1998) Clustered organization and transcriptional analysis of a family of five csp genes of Lactococcus lactis MG1363. Microbiology 144: 2885–2893.

    Google Scholar 

  • Wouters J A, Jeynov B, Rombouts F M, de Vos W M, Kuipers O P& Abee T (1999a) Analysis of the role of 7 kDa cold-shock proteins of Lactococcus lactis MG1363 in cryoprotection. Microbiology 145: 3185–3194.

    Google Scholar 

  • Wouters J A, Rombouts F M, de Vos W M, Kuipers O P& Abee T (1999b) Cold shock proteins and low-temperature response of Streptococcus thermophilus CNRZ302. Appl. Environ. Microbiol. 65: 4436–4442.

    Google Scholar 

  • Wouters J A, Kamphuis H H, Hugenholtz J, Kuipers O P, de Vos W M& Abee T (2000a) Changes in glycolytic activity of Lactococcus lactis induced by low temperature. Appl. Environ. Microbiol. 66: 3686–3691.

    Google Scholar 

  • Wouters J A, Mailhes M, Rombouts F M, de Vos W M, Kuipers O P& Abee T (2000b) Physiological and regulatory effects of controlled overproduction of five cold shock proteins of Lactococcus lactis MG1363. Appl. Environ. Microbiol. 66: 3756–3763.

    Google Scholar 

  • Wouters J A, Rombouts F M, Kuipers O P, de Vos W M& Abee T (2000c) The role of cold-shock proteins in low-temperature adaptation of food-related bacteria [In Process Citation]. Syst. Appl. Microbiol. 23: 165–173.

    Google Scholar 

  • Xia B, Ke H& Inouye M (2001) Acquirement of cold sensitivity by quadruple deletion of the cspA family and its suppression by PNPase S1 domain in Escherichia coli. Mol.Microbiol. 40: 179–188.

    Google Scholar 

  • Yamamoto N, Masujima Y& Takano T (1996) Reduction of membrane bound ATPase activity in a Lactobacillus helveticus strain with slower growth at low pH. FEMS Microbiol. Rev. 138: 179–184.

    Google Scholar 

  • Yamanaka K, Fang L& Inouye M (1998) The CspA family in Escherichia coli: multiple gene duplication for stress adaptation. Mol. Microbiol. 27: 247–255.

    Google Scholar 

  • Yamanaka K, Mitta M& Inouye M (1999) Mutation analysis of the 5' untranslated region of the cold shock cspA mRNA of Escherichia coli. J. Bacteriol. 181: 6284–6291.

    Google Scholar 

  • Yamashita Y, Takehara T& Kuramitsu H K (1993) Molecular characterization of a Streptococcus mutans mutant altered in environmental stress responses. J. Bacteriol. 175: 6220–6228.

    Google Scholar 

  • Yi X, Kot E& Bezkorovainy A (1998) Properties of NADH oxidase from Lactobacillus delbrueckii ssp. bulgaricus. J. Sci. Food Agric. 78: 527–534.

    Google Scholar 

  • Yokota A, Amachi S, Ishii S& Tomita F (1995) Acid sensitivity of a mutan of Lactococcus lactis subsp. lactis C2 with reduced membrane bound ATPase activity. Biosci. Biotech. Biochem. 59: 2004–2007.

    Google Scholar 

  • Yokota A, Veenstra M, Kurdi P, van Veen H W& Konings W N (2000) Cholate resistance in Lactococcus lactis is mediated by an ATP-dependent multispecific organic anion transporter. J. Bacteriol. 182: 5196–5201.

    Google Scholar 

  • Yura T, Kanemori M& Morita T M (2000) The heat shock response: regulation and function. In: Storz G& Hengge-Aronis R (Eeds.) Bacterial Stress Responses (pp 3–18). ASM Press, Washington, DC.

    Google Scholar 

  • Zhu M, Takenaka S, Sato M& Hoshino E (2001) Influence of starvation and biofilm formation on acid resistance of Streptococcus mutans. Oral Microbiol. Immunol. 16: 24–27.

    Google Scholar 

  • Zuber U& Schumann W (1994) CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J. Bacteriol. 176: 1359–1363.

    Google Scholar 

  • Zuniga M, Champomier-Verges M, Zagorec M& Perez-Martinez G (1998) Structural and functional analysis of the gene cluster encoding the enzymes of the arginine deiminase pathway of Lactobacillus sake. J. Bacteriol. 180: 4154–4159.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Emmanuelle Maguin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

van de Guchte, M., Serror, P., Chervaux, C. et al. Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 82, 187–216 (2002). https://doi.org/10.1023/A:1020631532202

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020631532202

Navigation