Environmental stress responses in Lactobacillus: A review

Environmental stress responses in Lactobacillus, which have been investigated mainly by proteomics approaches, are reviewed. The physiological and molecular mechanisms of responses to heat, cold, acid, osmotic, oxygen, high pressure and starvation stresses are described. Specific examples of the repercussions of these effects in food processing are given. Molecular mechanisms of stress responses in lactobacilli and other bacteria are compared.

[1]  R. Kirby,et al.  Evidence of membrane damage in Lactobacillus bulgaricus following freeze drying , 1997 .

[2]  Y. Auffray,et al.  Starvation-Induced Stress Resistance in Lactococcus lactis subsp. lactis IL1403 , 1994, Applied and environmental microbiology.

[3]  Y. Auffray,et al.  Starvation and osmotic stress induced multiresistances. Influence of extracellular compounds. , 2000, International journal of food microbiology.

[4]  C. Oberg,et al.  Characterization of the Lactobacillus helveticus groESL operon. , 1998, Research in microbiology.

[5]  B. Poolman,et al.  Osmotic regulation of intracellular solute pools in Lactobacillus plantarum , 1996, Journal of bacteriology.

[6]  M. Giambiagi-deMarval,et al.  Expression of the Major Heat Shock Proteins DnaK and GroEL in Streptococcus pyogenes: A Comparison to Enterococcus faecalis and Staphylococcus aureus , 2001, Current Microbiology.

[7]  A. Kelly,et al.  Use of Hydrostatic Pressure for Inactivation of Microbial Contaminants in Cheese , 2000, Applied and Environmental Microbiology.

[8]  R. Raya,et al.  Adaptive acid tolerance response in Lactobacillus acidophilus , 1998, Biotechnology Letters.

[9]  M. Guéguen,et al.  Cryoprotectants lead to phenotypic adaptation to freeze-thaw stress in Lactobacillus delbrueckii ssp. bulgaricus CIP 101027T. , 2000, Cryobiology.

[10]  Antioxidative properties of Lactobacillus sake upon exposure to elevated oxygen concentrations. , 2001, FEMS microbiology letters.

[11]  M. Zagorec,et al.  Development of Genetic Tools forLactobacillus sakei: Disruption of the β-Galactosidase Gene and Use of lacZ as a Reporter Gene To Study Regulation of the Putative Copper ATPase, AtkB , 2000, Applied and Environmental Microbiology.

[12]  R. Rowbury,et al.  PhoE porin of Escherichia coli and phosphate reversal of acid damage and killing and of acid induction of the CadA gene product. , 1993, The Journal of applied bacteriology.

[13]  Yun-Ji Kim,et al.  Acid Tolerance ofLactobacillus plantarumfromKimchi , 1999 .

[14]  W. Hammes,et al.  Utilization of electron acceptors by lactobacilli isolated from sourdough , 1995 .

[15]  J. Hoheisel,et al.  Global Analysis of the General Stress Response ofBacillus subtilis , 2001, Journal of bacteriology.

[16]  A. Margolles,et al.  Hop Resistance in the Beer Spoilage Bacterium Lactobacillus brevis Is Mediated by the ATP-Binding Cassette Multidrug Transporter HorA , 2001, Journal of bacteriology.

[17]  S. Blum,et al.  Food processing: probiotic microorganisms for beneficial foods. , 2001, Current opinion in biotechnology.

[18]  R. Gómez,et al.  Effect of High Pressure on the Viability and Enzymatic Activity of Mesophilic Lactic Acid Bacteria Isolated from Caprine Cheese , 1999 .

[19]  M. Yamasaki,et al.  Hop-resistant Lactobacillus brevis contains a novel plasmid harboring a multidrug resistance-like gene , 1997 .

[20]  C. F. Strittmatter Flavin-linked oxidative enzymes of Lactobacillus casei. , 1959, The Journal of biological chemistry.

[21]  B. Poolman,et al.  Glycine Betaine Transport in Lactococcus lactis Is Osmotically Regulated at the Level of Expression and Translocation Activity , 2000, Journal of bacteriology.

[22]  W. Hammes,et al.  Oxygen-Dependent Regulation of the Expression of the Catalase Gene katA of Lactobacillus sakei LTH677 , 1998, Applied and Environmental Microbiology.

[23]  A Schulz,et al.  hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes , 1996, Journal of bacteriology.

[24]  Bernd Bukau,et al.  The Hsp70 and Hsp60 Chaperone Machines , 1998, Cell.

[25]  A. Amanatidou,et al.  Superoxide dismutase plays an important role in the survival of Lactobacillus sake upon exposure to elevated oxygen , 2001, Archives of Microbiology.

[26]  W. Holzapfel,et al.  Lactic acid bacteria of foods and their current taxonomy. , 1997, International journal of food microbiology.

[27]  B. Mayo,et al.  Cloning and characterization of cspL and cspP, two cold-inducible genes from Lactobacillus plantarum , 1997, Journal of bacteriology.

[28]  J. Piard,et al.  Inhibiting factors produced by lactic acid bacteria. 1. Oxygen metabolites and catabolism end-products , 1991 .

[29]  S. Condon,et al.  Responses of lactic acid bacteria to oxygen , 1987 .

[30]  J. G. Morris,et al.  The effects of aeration on the bioreductive abilities of some heterofermentative lactic acid bacteria , 1995 .

[31]  L. Rensing,et al.  The cytoplasmic pH, ATP content and total protein synthesis rate during heat-shock protein inducing treatments in yeast. , 1987, Experimental cell research.

[32]  A. P. DE Ruiz Holgado,et al.  Effect of Drying Medium on Residual Moisture Content and Viability of Freeze-Dried Lactic Acid Bacteria , 1985, Applied and environmental microbiology.

[33]  G. Jan,et al.  Lactobacillus delbrueckii ssp. bulgaricus thermotolerance , 2001 .

[34]  M. Turner,et al.  The bspA Locus of Lactobacillus fermentum BR11 Encodes an l-Cystine Uptake System , 1999, Journal of bacteriology.

[35]  S. Shimamura,et al.  Effects of Pressure on Enzyme Activities of Lactobacillus helveticus LHE-511 , 1994 .

[36]  C. Oberg,et al.  Attributes of the Heat Shock Response in Three Species of Dairy Lactobacillus , 1997 .

[37]  M. Inouye,et al.  Cold shock and adaptation , 1998, BioEssays : news and reviews in molecular, cellular and developmental biology.

[38]  M. Skinner,et al.  Expression of clpX, an ATPase subunit of the Clp protease, is heat and cold shock inducible in Lactococcus lactis. , 2001, Journal of dairy science.

[39]  G. Rapoport,et al.  CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram‐positive bacteria , 1999, Molecular microbiology.

[40]  M. Marahiel,et al.  A superfamily of proteins that contain the cold-shock domain. , 1998, Trends in biochemical sciences.

[41]  C. Dunne,et al.  Variation in Resistance to Hydrostatic Pressure among Strains of Food-Borne Pathogens , 1999, Applied and Environmental Microbiology.

[42]  W. Hammes,et al.  Cloning, sequence, and phenotypic expression of katA, which encodes the catalase of Lactobacillus sake LTH677 , 1992, Applied and environmental microbiology.

[43]  M. Inouye,et al.  The CspA family in Escherichia coli : multiple gene duplication for stress adaptation , 1998, Molecular microbiology.

[44]  G. Buettner,et al.  Endogenous Superoxide Dismutase Levels Regulate Iron-Dependent Hydroxyl Radical Formation in Escherichia coli Exposed to Hydrogen Peroxide , 1998, Journal of bacteriology.

[45]  Y. Auffray,et al.  Physiological response of Enterococcus faecalis JH2‐2 to cold shock: growth at low temperatures and freezing/thawing challenge , 1996, Letters in applied microbiology.

[46]  L. Bini,et al.  The acid-stress response in Lactobacillus sanfranciscensis CB1. , 2001, Microbiology.

[47]  M. C. Manca de Nadra,et al.  Arginine dihydrolase pathway in Lactobacillus plantarum from orange. , 1999, International journal of food microbiology.

[48]  E. O'Sullivan,et al.  Intracellular pH is a major factor in the induction of tolerance to acid and other stresses in Lactococcus lactis , 1997, Applied and environmental microbiology.

[49]  R. Hutkins,et al.  pH Homeostasis in Lactic Acid Bacteria , 1993 .

[50]  K. Devine,et al.  New Family of Regulators in the Environmental Signaling Pathway Which Activates the General Stress Transcription Factor ςB of Bacillus subtilis , 2001, Journal of bacteriology.

[51]  H. Aso,et al.  Lactococcus lactis contains only one glutamate decarboxylase gene. , 1999, Microbiology.

[52]  T. Klaenhammer,et al.  The groESL Chaperone Operon ofLactobacillus johnsonii , 1999, Applied and Environmental Microbiology.

[53]  G. Jan,et al.  Two-Dimensional Electrophoresis Study of Lactobacillus delbrueckii subsp. bulgaricus Thermotolerance , 2002, Applied and Environmental Microbiology.

[54]  W. Kim,et al.  Assessment of Stress Response of the Probiotic Lactobacillus acidophilus , 2001, Current Microbiology.

[55]  K. Lewis,et al.  Emr, an Escherichia coli locus for multidrug resistance. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[56]  M. Pallen,et al.  The HtrA family of serine proteases , 1997, Molecular microbiology.

[57]  Boris Martinac,et al.  Mechanosensitive ion channels of E. coli activated by amphipaths , 1990, Nature.

[58]  R. P. Ross,et al.  Environmental adaptation of probiotic lactobacilli towards improvement of performance during spray drying , 2001 .

[59]  Claude P. Champagne,et al.  The Freeze-Drying of Lactic Acid Bacteria. A Review , 1991 .

[60]  W. D. de Vos,et al.  Cold Shock Proteins of Lactococcus lactis MG1363 Are Involved in Cryoprotection and in the Production of Cold-Induced Proteins , 2001, Applied and Environmental Microbiology.

[61]  E. O'Sullivan,et al.  Relationship between Acid Tolerance, Cytoplasmic pH, and ATP and H+-ATPase Levels in Chemostat Cultures of Lactococcus lactis , 1999, Applied and Environmental Microbiology.

[62]  L. Grivell,et al.  ATP-dependent proteases that also chaperone protein biogenesis. , 1997, Trends in biochemical sciences.

[63]  R. Lanciotti,et al.  Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. , 2001, Microbiology.

[64]  J. Foster,et al.  Adaptive acid tolerance response (ATR) in Aeromonas hydrophila. , 1994, Microbiology.

[65]  S. Ehrlich,et al.  Identification of stress‐inducible proteins in Lactobacillus delbrueckii subsp. bulgaricus , 2000, Electrophoresis.

[66]  P. Maloney,et al.  Exchange of Aspartate and Alanine , 1996, The Journal of Biological Chemistry.

[67]  J. Gaillard,et al.  Expression of a New Cold Shock Protein of 21.5 kDa and of the Major Cold Shock Protein by Streptococcus thermophilus After Cold Shock , 1999, Current Microbiology.

[68]  B. Poolman,et al.  Physiological Response of Lactobacillus plantarum to Salt and Nonelectrolyte Stress , 1998, Journal of bacteriology.

[69]  M. Putman,et al.  Molecular Properties of Bacterial Multidrug Transporters , 2000, Microbiology and Molecular Biology Reviews.

[70]  N. Russell,et al.  A comparison of thermal adaptation of membrane lipids in psychrophilic and thermophilic bacteria , 1990 .

[71]  P. Piper,et al.  Hsp30, the integral plasma membrane heat shock protein of Saccharomyces cerevisiae, is a stress-inducible regulator of plasma membrane H(+)-ATPase. , 1997, Cell stress & chaperones.

[72]  Maarten van de Guchte,et al.  Stress responses in lactic acid bacteria , 2002 .

[73]  T. Robinson,et al.  Variation in Resistance of Natural Isolates ofEscherichia coli O157 to High Hydrostatic Pressure, Mild Heat, and Other Stresses , 1999, Applied and Environmental Microbiology.

[74]  C. Shearman,et al.  Cloning and sequence analysis of the dnaK gene region of Lactococcus lactis subsp. lactis. , 1993, Journal of general microbiology.

[75]  K. Francis,et al.  Changes in cspL, cspP, and cspCmRNA Abundance as a Function of Cold Shock and Growth Phase inLactobacillus plantarum , 2000, Journal of bacteriology.

[76]  F. Franks,et al.  Protein destabilization at low temperatures. , 1995, Advances in protein chemistry.

[77]  P. Varmanen,et al.  Molecular Characterization of a Stress-Inducible Gene from Lactobacillus helveticus , 1998 .

[78]  W. D. de Vos,et al.  The role of cold-shock proteins in low-temperature adaptation of food-related bacteria. , 2000, Systematic and applied microbiology.

[79]  G T Montelione,et al.  Solution NMR structure and backbone dynamics of the major cold-shock protein (CspA) from Escherichia coli: evidence for conformational dynamics in the single-stranded RNA-binding site. , 1998, Biochemistry.

[80]  R. Hutkins,et al.  Proton-Translocating Adenosine Triphosphatase Activity in Lactic Acid Bacterial , 1991 .

[81]  M. Marahiel,et al.  Mutational analysis of the putative nucleic acid‐binding surface of the cold‐shock domain, CspB, revealed an essential role of aromatic and basic residues in binding of single‐stranded DNA containing the Y‐box motif , 1995, Molecular microbiology.

[82]  F. Vogensen,et al.  Disruption and Analysis of the clpB,clpC, and clpE Genes in Lactococcus lactis: ClpE, a New Clp Family in Gram-Positive Bacteria , 1999, Journal of bacteriology.

[83]  T. Abee,et al.  Microbial stress response in minimal processing. , 1999, International journal of food microbiology.

[84]  Q. Gu,et al.  Multicopy suppressors of prc mutant Escherichia coli include two HtrA (DegP) protease homologs (HhoAB), DksA, and a truncated R1pA , 1996, Journal of bacteriology.

[85]  Tatsuo Tanaka,et al.  Application of Hydrostatic Pressure to Yoghurt to Prevent its After-acidification , 1992 .

[86]  G. Venemâ,et al.  Environmental stress responses in Lactococcus lactis , 1999 .

[87]  B. Poolman,et al.  Mechanism of Osmotic Activation of the Quaternary Ammonium Compound Transporter (QacT) of Lactobacillus plantarum , 1998, Journal of bacteriology.

[88]  J. Smelt,et al.  Effects of High Pressure on Inactivation Kinetics and Events Related to Proton Efflux in Lactobacillus plantarum , 1998, Applied and Environmental Microbiology.

[89]  Y. Auffray,et al.  The Lactic Acid Stress Response of Lactococcus lactis subsp. lactis , 1996, Current Microbiology.

[90]  M. Inouye,et al.  CspA, the Major Cold-shock Protein of Escherichia coli, Is an RNA Chaperone* , 1997, The Journal of Biological Chemistry.

[91]  K. Schleifer,et al.  Phylogeny of the Genus Lactobacillus and Related Genera , 1995 .

[92]  P. Teixeira,et al.  Identification of sites of injury in Lactobacillus bulgaricus during heat stress , 1997, Journal of applied microbiology.

[93]  M. Jobin,et al.  Expression of the Oenococcus oeni trxA gene is induced by hydrogen peroxide and heat shock. , 1999, Microbiology.

[94]  Michael H. W. Weber,et al.  CSDBase: an interactive database for cold shock domain-containing proteins and the bacterial cold shock response , 2002, Nucleic Acids Res..

[95]  S. Ehrlich,et al.  Relationships between arginine degradation, pH and survival in Lactobacillus sakei. , 1999, FEMS microbiology letters.

[96]  B. Weimer,et al.  Isolation and characterization of acid- and bile-tolerant isolates from strains of Lactobacillus acidophilus. , 1999, Journal of dairy science.

[97]  W. Verstraete,et al.  Significance of bile salt hydrolytic activities of lactobacilli. , 1995, The Journal of applied bacteriology.

[98]  T. Shellhammer,et al.  Effects of High Pressure on the Viability, Morphology, Lysis, and Cell Wall Hydrolase Activity of Lactococcus lactis subsp. cremoris , 2002, Applied and Environmental Microbiology.

[99]  F. Neidhardt,et al.  Stress response of Escherichia coli to elevated hydrostatic pressure , 1993, Journal of bacteriology.

[100]  W. D. de Vos,et al.  Cold Shock Proteins and Low-Temperature Response ofStreptococcus thermophilus CNRZ302 , 1999, Applied and Environmental Microbiology.

[101]  R. Vogel,et al.  Effects of High Pressure on Survival and Metabolic Activity of Lactobacillus plantarum TMW1.460 , 2000, Applied and Environmental Microbiology.

[102]  B. Poolman,et al.  Regulation of compatible solute accumulation in bacteria , 1998, Molecular microbiology.

[103]  M. Hecker,et al.  Heat‐shock and general stress response in Bacillus subtilis , 1996, Molecular microbiology.

[104]  I. Fridovich Fundamental Aspects of Reactive Oxygen Species, or What's the Matter with Oxygen? , 1999, Annals of the New York Academy of Sciences.

[105]  J. Garel,et al.  Increased Production of Hydrogen Peroxide byLactobacillus delbrueckii subsp. bulgaricus upon Aeration: Involvement of an NADH Oxidase in Oxidative Stress , 2000, Applied and Environmental Microbiology.

[106]  M. Sanders Summary of conclusions from a consensus panel of experts on health attributes of lactic cultures: significance to fluid milk products containing cultures. , 1993, Journal of dairy science.

[107]  M. Inouye,et al.  Cold-shock response and cold-shock proteins. , 1999, Current opinion in microbiology.

[108]  J. Hoch,et al.  Control of the initiation of sporulation in Bacillus subtilis by a phosphorelay. , 1991, Research in microbiology.

[109]  H. Ingmer,et al.  ClpP participates in the degradation of misfolded protein in Lactococcus lactis , 1999, Molecular microbiology.

[110]  A. Delgado,et al.  In Situ Determination of the Intracellular pH of Lactococcus lactis and Lactobacillus plantarum during Pressure Treatment , 2002, Applied and Environmental Microbiology.

[111]  A. Görg,et al.  High pressure effects step‐wise altered protein expression in Lactobacillus sanfranciscensis , 2002, Proteomics.

[112]  M. R. Stuart,et al.  Influence of Carbohydrate Starvation and Arginine on Culturability and Amino Acid Utilization of Lactococcus lactis subsp. lactis , 1999, Applied and Environmental Microbiology.

[113]  Shaoquan Liu,et al.  A REVIEW : Arginine metabolism in wine lactic acid bacteria and its practical significance , 1998 .

[114]  Y. M. Lee,et al.  Threonine phosphorylation of modulator protein RsbR governs its ability to regulate a serine kinase in the environmental stress signaling pathway of Bacillus subtilis. , 1999, Journal of molecular biology.

[115]  G. Jayaraman,et al.  Transcriptional analysis of the Streptococcus mutans hrcA, grpE and dnaK genes and regulation of expression in response to heat shock and environmental acidification , 1997, Molecular microbiology.

[116]  W. D. de Vos,et al.  Analysis of the role of 7 kDa cold-shock proteins of Lactococcus lactis MG1363 in cryoprotection. , 1999, Microbiology.

[117]  C Kung,et al.  Mechanosensitive channels of Escherichia coli: the MscL gene, protein, and activities. , 1997, Annual review of physiology.

[118]  C. Gahan,et al.  Two-Dimensional Polyacrylamide Gel Electrophoresis Analysis of the Acid Tolerance Response in Listeria monocytogenes LO28 , 1997, Applied and environmental microbiology.

[119]  P. Fox,et al.  Arginine Catabolism by Sourdough Lactic Acid Bacteria: Purification and Characterization of the Arginine Deiminase Pathway Enzymes from Lactobacillus sanfranciscensis CB1 , 2002, Applied and Environmental Microbiology.

[120]  T. Cogan,et al.  Heat resistance of Lactobacillus spp. isolated from Cheddar cheese , 1999, Letters in applied microbiology.

[121]  W. Hammes,et al.  Molecular characterisation of the dnaK operon of Lactobacillus sakei LTH681. , 1999, Systematic and applied microbiology.

[122]  K. Schleifer,et al.  Purification and biochemical characterization of pyruvate oxidase from Lactobacillus plantarum , 1984, Journal of bacteriology.

[123]  W. D. de Vos,et al.  Clustered organization and transcriptional analysis of a family of five csp genes of Lactococcus lactis MG1363. , 1998, Microbiology.

[124]  G. Bender,et al.  Arginine deiminase system and bacterial adaptation to acid environments , 1987, Applied and environmental microbiology.

[125]  A. Driessen,et al.  Generation of a proton motive force by histidine decarboxylation and electrogenic histidine/histamine antiport in Lactobacillus buchneri , 1993, Journal of bacteriology.

[126]  K. Francis,et al.  Detection and speciation of bacteria through PCR using universal major cold-shock protein primer oligomers , 1997, Journal of Industrial Microbiology and Biotechnology.

[127]  D. Landsman RNP-1, an RNA-binding motif is conserved in the DNA-binding cold shock domain. , 1992, Nucleic acids research.

[128]  R. F. Vogel,et al.  Effects of Pressure-Induced Membrane Phase Transitions on Inactivation of HorA, an ATP-Dependent Multidrug Resistance Transporter, in Lactobacillus plantarum , 2002, Applied and Environmental Microbiology.

[129]  J. Saunders,et al.  13C incorporation into DNA as a means of identifying the active components of ammonia‐oxidizer populations , 2001, Letters in applied microbiology.

[130]  E. Maguin,et al.  Lactococcus lactis and stress , 1996, Antonie van Leeuwenhoek.

[131]  Adaptation of Lactobacillus alimentarius to environmental stresses. , 2000, International journal of food microbiology.

[132]  A. Neyfakh,et al.  Efflux-mediated drug resistance in Gram-positive bacteria. , 2001, Current opinion in microbiology.

[133]  G. Lorca,et al.  A Low-pH-Inducible, Stationary-Phase Acid Tolerance Response in Lactobacillus acidophilus CRL 639 , 2001, Current Microbiology.

[134]  E. Ron,et al.  Regulation and organization of the groE and dnaK operons in Eubacteria. , 1996, FEMS microbiology letters.

[135]  D. Pridmore,et al.  Impact of multiple stress factors on the survival of dairy lactobacilli. , 2000 .

[136]  K. Horikoshi,et al.  High pressure influences on gene and protein expression. , 1995, Research in microbiology.

[137]  S. Lindquist,et al.  The heat-shock proteins. , 1988, Annual review of genetics.

[138]  F. Götz,et al.  Oxygen utilization by Lactobacillus plantarum , 1980, Archives of Microbiology.

[139]  A. Yamaguchi,et al.  Analysis of a Complete Library of Putative Drug Transporter Genes in Escherichia coli , 2001, Journal of bacteriology.

[140]  J. Foster,et al.  Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium , 1991, Journal of bacteriology.

[141]  H. Siegumfeldt,et al.  Dynamic Changes of Intracellular pH in Individual Lactic Acid Bacterium Cells in Response to a Rapid Drop in Extracellular pH , 2000, Applied and Environmental Microbiology.

[142]  D. Savage,et al.  Bile Salt Hydrolase Activity and Resistance to Toxicity of Conjugated Bile Salts Are Unrelated Properties in Lactobacilli , 2001, Applied and Environmental Microbiology.

[143]  N. Sauvageot,et al.  Characterization of Lactobacillus collinoides response to heat, acid and ethanol treatments , 1999, Applied Microbiology and Biotechnology.

[144]  P. Blanc,et al.  Study of the cryotolerance of Lactobacillus acidophilus: effect of culture and freezing conditions on the viability and cellular protein levels. , 2000, International journal of food microbiology.

[145]  J. Gaze,et al.  Heat resistance of Bacillus cereus, Salmonella typhimurium and Lactobacillus delbrueckii in relation to pH and ethanol. , 2001, International journal of food microbiology.

[146]  B. Poolman,et al.  Glycine Betaine Fluxes in Lactobacillus plantarum during Osmostasis and Hyper- and Hypo-osmotic Shock (*) , 1996, The Journal of Biological Chemistry.

[147]  P Youngman,et al.  Genome‐wide analysis of the general stress response in Bacillus subtilis , 2001, Molecular microbiology.

[148]  W. D. de Vos,et al.  Cloning, nucleotide sequence, and regulatory analysis of the Lactococcus lactis dnaJ gene , 1993, Journal of bacteriology.

[149]  R. Pagán,et al.  Relationship between Membrane Damage and Cell Death in Pressure-Treated Escherichia coli Cells: Differences between Exponential- and Stationary-Phase Cells and Variation among Strains , 2000, Applied and Environmental Microbiology.

[150]  M. Gobbetti,et al.  Lactobacillus sanfranciscensis CB1: manganese, oxygen, superoxide dismutase and metabolism , 1999, Applied Microbiology and Biotechnology.

[151]  G. Bender,et al.  Membrane ATPases and acid tolerance of Actinomyces viscosus and Lactobacillus casei , 1987, Applied and environmental microbiology.

[152]  A. Lepeuple,et al.  Characterization of cspB, a cold-shock-inducible gene from Lactococcus lactis, and evidence for a family of genes homologous to the Escherichia coli cspA major cold shock gene , 1997, Journal of bacteriology.

[153]  G. Pérez-Martínez,et al.  Structural and Functional Analysis of the Gene Cluster Encoding the Enzymes of the Arginine Deiminase Pathway ofLactobacillus sake , 1998, Journal of bacteriology.

[154]  F. Hartl,et al.  Molecular chaperone functions of heat-shock proteins. , 1993, Annual review of biochemistry.

[155]  W. D. de Vos,et al.  Physiological and Regulatory Effects of Controlled Overproduction of Five Cold Shock Proteins of Lactococcus lactisMG1363 , 2000, Applied and Environmental Microbiology.

[156]  I. Fridovich,et al.  Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria , 1981, Journal of bacteriology.

[157]  G. Montelione,et al.  Solution NMR structure of the major cold shock protein (CspA) from Escherichia coli: identification of a binding epitope for DNA. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[158]  W. Kim,et al.  Identification of a Cold Shock Gene in Lactic Acid Bacteria and the Effect of Cold Shock on Cryotolerance , 1997, Current Microbiology.

[159]  E. R. Kashket Bioenergetics of lactic acid bacteria: cytoplasmic pH and osmotolerance , 1987 .

[160]  Oscar P. Kuipers,et al.  Changes in Glycolytic Activity of Lactococcus lactis Induced by Low Temperature , 2000, Applied and Environmental Microbiology.

[161]  P. Piper Molecular events associated with acquisition of heat tolerance by the yeast Saccharomyces cerevisiae. , 1993, FEMS microbiology reviews.

[162]  M. Inouye,et al.  Escherichia coli CspA-family RNA chaperones are transcription antiterminators. , 2000, Proceedings of the National Academy of Sciences of the United States of America.