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Antonie van Leeuwenhoek

, Volume 82, Issue 1–4, pp 187–216 | Cite as

Stress responses in lactic acid bacteria

  • Maarten van de Guchte
  • Pascale Serror
  • Christian Chervaux
  • Tamara Smokvina
  • Stanislav D. Ehrlich
  • Emmanuelle Maguin
Article

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.

lactic acid bacteria stress response adaptive response cross protection gene regulation 

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References

  1. Abdelal A T (1979) Arginine catabolism by microorganisms. Annu Rev Microbiol. 33: 139–168.Google Scholar
  2. 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
  3. 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
  4. Archibald F S& Fridovich I (1981) Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria. J Bacteriol. 146: 928–936.Google Scholar
  5. 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
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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
  11. 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
  12. 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
  13. Bakker E P& Harold F M (1980) Energy coupling to potassium transport in Streptococcus faecalis. J. Biol. Chem. 255: 433–440.Google Scholar
  14. 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
  15. 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
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. Broadbent J R, Oberg C J& Wei L (1998) Characterization of the Lactobacillus helveticus groESL operon. Res. Microbiol. 149: 247–253.Google Scholar
  28. 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
  29. 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
  30. 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
  31. 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
  32. 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).Google Scholar
  33. 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
  34. 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
  35. 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
  36. Chatterji D& Ojha A K (2001) Revisiting the stringent response, ppGpp and starvation signaling. Curr. Opin. Microbiol. 4: 160–165.Google Scholar
  37. 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
  38. 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
  39. Condon S (1987) Responses of lactic acid bacteria to oxygen. FEMS Microbiol. Rev. 46: 269–280.Google Scholar
  40. Chen Y Y, Weaver C A& Burne R A (2000) Dual functions of Streptococcus salivarius urease. J. Bacteriol. 182: 4667–4669.Google Scholar
  41. 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
  42. Crow V L& Thomas T D (1982) Arginine metabolism in lactic Streptococci. J. Bacteriol. 150: 1024–1032.Google Scholar
  43. Csonka L N& Hanson A D (1991) Prokaryotic osmoregulation: genetics and physiology. Annu. Rev. Microbiol. 45: 569–606.Google Scholar
  44. Cunin R, Glansdorff N, Pierard A& Stalon V (1986) Biosynthesis and metabolism of arginine in bacteria. Microbiol. Rev. 50: 314–352.Google Scholar
  45. 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
  46. 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
  47. 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
  48. 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
  49. 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
  50. 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
  51. 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
  52. 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
  53. 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
  54. 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
  55. 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
  56. 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
  57. 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
  58. 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
  59. 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
  60. 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
  61. Engesser D M& Hammes W P (1994) Non-heme catalase activity of lactic acid bacteria. Syst. Appl. Microbiol. 17: 11–19.Google Scholar
  62. 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
  63. 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
  64. 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
  65. 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
  66. 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
  67. Fitzgerald J R& Musser J M (2001) Evolutionary genomics of pathogenic bacteria. Trends Microbiol. 9: 547–553.Google Scholar
  68. 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
  69. 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
  70. Foucaud-Sceunemann C&Poquet I (2002) The Lactococcus lactis HtrA protease is induced and essential for cell survival under stress conditions. In preparation.Google Scholar
  71. 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
  72. Frees D& Ingmer H (1999) ClpP participates in the degradation of misfolded protein in Lactococcus lactis. Mol. Microbiol. 31: 79–87.Google Scholar
  73. 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
  74. 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
  75. Galperin M Y, Walker D R& Koonin E V (1998) Analogous enzymes: independent inventions in enzyme evolution. Genome Res. 8: 779–790.Google Scholar
  76. 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
  77. 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
  78. 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
  79. 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
  80. 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
  81. 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
  82. Glaasker E, Konings W N& Poolman B (1996b) Osmotic regulation of intracellular solute pools in Lactobacillus plantarum. J. Bacteriol. 178: 575–582.Google Scholar
  83. 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
  84. 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
  85. 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
  86. 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
  87. 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
  88. 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
  89. 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
  90. 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
  91. 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
  92. 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
  93. 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
  94. 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
  95. Gunn J S (2000) Mechanisms of bacterial resistance and response to bile. Microbes Infect. 2: 907–913.Google Scholar
  96. 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
  97. 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
  98. 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
  99. 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
  100. 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
  101. 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
  102. 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
  103. 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
  104. 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
  105. Harper D S& Loesche W J (1984) Growth and acid tolerance of human dental plaque bacteria. Arch. Oral Biol. 29: 843–848.Google Scholar
  106. 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
  107. 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
  108. 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
  109. 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
  110. 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
  111. 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
  112. 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
  113. 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
  114. Higgins C F (1992) ABC transporters: from microorganisms toman. Annu. Rev. Cell Biol. 8: 67–113.Google Scholar
  115. Higuchi T, Hayashi H& Abe K (1997) Exchange of glutamate and gamma-aminobutyrate in a Lactobacillus strain. J. Bacteriol. 179: 3362–3364.Google Scholar
  116. 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
  117. Hutkins R W& Nannen N L (1993) pH homeostasis in lactic acid bacteria. J. Dairy Sci. 76: 2354–2365.Google Scholar
  118. 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
  119. Igarashi T, Kono Y& Tanaka K (1996) Molecular cloning of manganese catalase from Lactobacillus plantarum. J. Biol. Chem. 271: 29521–29524.Google Scholar
  120. 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
  121. Irvine A S& Guest J R (1993) Lactobacillus casei contains a member of the CRP-FNR family. Nucleic Acids Res. 21: 753.Google Scholar
  122. 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
  123. 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
  124. 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
  125. 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
  126. 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
  127. 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
  128. 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
  129. Kashket E R (1984) Bioenergetics of lactic acid bacteria: cytoplasmic pH and osmotolerance. FEMS Microbiol. Rev. 46: 233–244.Google Scholar
  130. 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
  131. 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
  132. 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
  133. Kim S G& Batt C A (1993) Cloning and sequencing of the Lactococcus lactis subsp. lactis groESL operon. Gene. 127: 121–126.Google Scholar
  134. 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
  135. 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
  136. 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
  137. 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
  138. 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
  139. Kobayashi H, Murakami N& Unemoto T (1982) Regulation of the cytoplasmic pH in Streptococcus faecalis. J. Biol. Chem. 257: 13246–13252.Google Scholar
  140. 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
  141. 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
  142. 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
  143. 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
  144. Kono Y& Fridovich I (1983) Isolation and characterization of the pseudocatalase of Lactobacillus plantarum. J. Biol. Chem. 258: 6015–6019.Google Scholar
  145. 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
  146. Kornberg A, Rao N N& Ault-Riche D (1999) Inorganic polyphosphate: a molecule of many functions. Annu. Rev. Biochem. 68: 89–125.Google Scholar
  147. 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
  148. 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
  149. 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
  150. 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
  151. 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
  152. 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
  153. 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
  154. Lawrence J G, Hendrix R W& Casjens S (2001) Where are the pseudogenes in bacterial genomes? Trends Microbiol. 9: 535–540.Google Scholar
  155. 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
  156. 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
  157. 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
  158. Lin M Y& Yen C L (1999) Antioxidative ability of lactic acid bacteria. J. Agric. Food Chem. 47: 1460–1466.Google Scholar
  159. Lindahl T& Nyberg B (1972) Rate of depurination of native deoxyribonucleic acid. Biochemistry 11: 3610–3618.Google Scholar
  160. 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
  161. 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
  162. 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
  163. 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
  164. 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
  165. 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
  166. Ma Y& Marquis R E (1997) Thermophysiology of Streptococcus mutans and related lactic-acid bacteria. Antonie Van Leeuwenhoek 72: 91–100.Google Scholar
  167. 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
  168. 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
  169. 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
  170. Markham P N& Neyfakh A A (2001) Efflux-mediated drug resistance in Gram-positive bacteria. Curr. Opin. Microbiol. 4: 509–514.Google Scholar
  171. 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
  172. 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
  173. 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
  174. 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
  175. 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
  176. 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
  177. 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
  178. 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
  179. Mercenier A, Muller-Alouf H& Grangette C (2000) Lactic acid bacteria as live vaccines. Curr. Issues Mol. Biol. 2: 17–25.Google Scholar
  180. 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.Google Scholar
  181. 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
  182. 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
  183. 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
  184. Nannen N L& Hutkins R W (1991) Proton translocating adenosine triphosphatase activity in lacic acid bacteria. J. Dairy Sci. 74: 747–751.Google Scholar
  185. 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
  186. 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
  187. 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
  188. 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
  189. 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
  190. 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
  191. 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
  192. 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
  193. 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
  194. 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
  195. 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
  196. 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
  197. 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
  198. 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
  199. 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
  200. 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
  201. 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
  202. 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
  203. 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
  204. Poolman B& Glaasker E (1998) Regulation of compatible solute accumulation in bacteria. Mol. Microbiol. 29: 397–407.Google Scholar
  205. 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
  206. 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
  207. 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
  208. 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
  209. 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
  210. 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
  211. 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
  212. 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
  213. 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
  214. 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
  215. Rallu F, Gruss A& Maguin E (1996) Lactococcus lactis and stress. Antonie van Leeuwenhoek 70: 243–251.Google Scholar
  216. 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
  217. 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
  218. Rastogi V K& Girvin M E (1999) Structural changes linked to proton translocation by subunit c of the ATP synthase. Nature 402: 263–268.Google Scholar
  219. Renault P, Gaillardin C& Heslot H (1988) Role of malolactic fermentation in lactic acid bacteria. Biochimie 70: 375–379.Google Scholar
  220. Rince A, Flahaut S& Auffray Y (2000) Identification of general stress genes in Enterococcus faecalis. Int. J. Food Microbiol. 55: 87–91.Google Scholar
  221. 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.Google Scholar
  222. Russell D W& Setchell K D (1992) Bile acid biosynthesis. Biochemistry 31: 4737–4749.Google Scholar
  223. 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
  224. 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
  225. 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
  226. 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
  227. 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
  228. Sancar A (1996) DNA excision repair. Annu. Rev. Biochem. 65: 43–81.Google Scholar
  229. 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
  230. 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
  231. 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
  232. Sanders J W, Venema G, Kok J (1999) Environmental stress responses in Lactococcus lactis. FEMS Microbiol. Rev. 23: 483–501.Google Scholar
  233. Schiffrin E J& Blum S (2001) Food processing: probiotic microorganisms for beneficial foods. Curr. Opin. Biotechnol. 12: 499–502.Google Scholar
  234. 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
  235. 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
  236. 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
  237. 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
  238. 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
  239. 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
  240. 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
  241. Smeds A, Varmanen P& Palva A (1998) Molecular characterization of a stress-inducible gene from Lactobacillus helveticus. J. Bacteriol. 180: 6148–6153.Google Scholar
  242. 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
  243. Somero G N (1995) Proteins and temperature. Annu. Rev. Physiol. 57: 43–68.Google Scholar
  244. 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
  245. 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
  246. Steiner K& Malke H (2001) relA-Independent amino acid starvation response network of Streptococcus pyogenes. J. Bacteriol. 183: 7354–7364.Google Scholar
  247. 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
  248. Stiles M E (1996) Biopreservation by lactic acid bacteria. Antonie Van Leeuwenhoek 70: 331–345.Google Scholar
  249. Stock D, Leslie A G& Walker J E (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286: 1700–1705.Google Scholar
  250. Stortz G& Hengge-Aronis R (Eds.) (2000) Bacterial Stress Responses (p 485). ASM Press, Washington, DC.Google Scholar
  251. 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
  252. 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: 11840–11843Google Scholar
  253. 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
  254. Takahashi N& Yamada T (1999) Acid-induced acid tolerance and acidogenicity of non-mutans streptococci. Oral Microbiol. Immunol. 14: 43–48.Google Scholar
  255. 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
  256. 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
  257. 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
  258. 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
  259. Thanassi D G, Cheng L W& Nikaido H (1997) Active efflux of bile salts by Escherichia coli. J. Bacteriol. 179: 2512–2518.Google Scholar
  260. 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
  261. 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
  262. 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
  263. 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
  264. 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
  265. 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
  266. 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
  267. 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
  268. 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
  269. 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
  270. 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
  271. 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
  272. 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
  273. 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
  274. 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
  275. 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
  276. 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
  277. 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
  278. 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
  279. 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
  280. 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
  281. 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
  282. 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
  283. 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
  284. 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
  285. 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
  286. 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
  287. 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
  288. 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
  289. 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
  290. 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
  291. 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
  292. 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
  293. 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
  294. 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
  295. 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
  296. 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
  297. 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
  298. 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
  299. 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
  300. 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
  301. 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
  302. 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
  303. 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
  304. 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
  305. 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
  306. 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

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Maarten van de Guchte
    • 1
  • Pascale Serror
    • 1
  • Christian Chervaux
    • 1
  • Tamara Smokvina
    • 1
  • Stanislav D. Ehrlich
    • 1
  • Emmanuelle Maguin
    • 1
  1. 1.Génétique Microbienne, INRAJouy en Josas CedexFrance

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