Skip to main content

Responses of Lactic Acid Bacteria to Cold Stress

  • Chapter
  • First Online:
Stress Responses of Lactic Acid Bacteria

Part of the book series: Food Microbiology and Food Safety ((FMFS))

Abstract

In response to temperature downshift, a number of changes occur in cellular physiology, such as a decrease in membrane fluidity, inefficient folding of some proteins, and hampered ribosome function. Cold stress leads to distinct responses depending on the actual temperature and in particular whether it is greater or less than 0°C. At subzero temperatures, which are associated with water freezing, the response of most prokaryotes is passive, leading slowly to death of the cells. This is associated with damage to the cell membrane and to DNA. Exposure to low temperatures above 0°C usually triggers an active response by bacteria typically based on the synthesis of specific proteins, generally called cold-shock proteins, to counteract the harmful effects of the temperature downshift, leading to a transient metabolic adaptation. Usually, the response is species or strain specific. Cold stress, which takes place during the cooling and freezing steps and throughout the frozen storage of industrial strains, is also the main cause of the loss of bacterial activity.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adam MM, Rana KJ, McAndrew BJ (1994) Effect of cryoprotectants on activity of selected enzymes in fish embryos. Cryobiol 32:92–104

    Article  Google Scholar 

  • Aguilar PS, Lopez P, de Mendoza D (1999) Transcriptional control of the low-temperature-inducible des gene, encoding the Δ5 desaturase of Bacillus subtilis. J Bacteriol 181:7028–7033

    CAS  Google Scholar 

  • Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC, De Mendoza D (2001) Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20:1681–1691

    Article  CAS  Google Scholar 

  • Ahrné S, Nobaek S, Jeppsson B, Adlerberth I, Wold AE, Molin G (1998) The normal Lactobacillus flora of healthy human rectal and oral mucosa. J Appl Microbiol 85:88–94

    Article  CAS  Google Scholar 

  • Bâati L, Fabre-Gea C, Auriol D, Blanc PJ (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

    Article  Google Scholar 

  • Beal C, Fonseca F, Corrieu G (2001) Resistance to freezing and frozen storage of Streptococcus thermophilus is related to membrane fatty acid composition. J Dairy Sci 84:2347–2356

    Article  CAS  Google Scholar 

  • Beckering C, Steil CL, Weber MWH, Volker U, Marahiel MA (2002) Genome wide transcriptional analysis of the cold shock response in Bacillus subtilis. J Bacteriol 184:6395–6402

    Article  CAS  Google Scholar 

  • Beaufilis S, Sauvageot N, Mazé A, Laplace JM, Auffray Y, Deutscher J, Hartke A (2007) The cold shock response of Lactobacillus casei: relation between HPr phosphorylation and resistance to freeze/thaw cycles. J Mol Microbiol Biotechnol 13:65–75

    Article  CAS  Google Scholar 

  • Brennan M, Wanismail B, Johnson MC, Ray B (1986) Cellular damage in dried Lactobacillus acidophilus. J Food Prot 49:47–53

    CAS  Google Scholar 

  • Broadbent JR, 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

    Article  CAS  Google Scholar 

  • Chastanet A, Ferrè T, Msadek T (2003) Comparative genomics reveal novel heat shock regulatory mechanisms in Staphylococcus aureus and other Gram-positive bacteria. Mol Microbiol 47:1061–1073

    Article  CAS  Google Scholar 

  • Chattopadhyay MK (2008) Cryotolerance in bacteria: interlink with adaptation to other stress factors. Trends Microbiol 16:455–460

    Article  CAS  Google Scholar 

  • Chouayekh H, Serror P, Boudebbouze S, Maguin E (2009) Highly efficient production of the staphylococcal nuclease reporter in Lactobacillus bulgaricus governed by the promoter of the hlbA gene. FEMS Microbiol Lett 293:232–239

    Article  CAS  Google Scholar 

  • Chu-Ky S, Tourdot-Marechal R, Marechal PA, Guzzo J (2005) Combined cold, acid, ethanol shocks in Oenococcus oeni: effects on membrane fluidity and cell viability. Biochim Biophys Acta 1717:118–124

    Article  CAS  Google Scholar 

  • Corcoran BM, Stanton C, Fitzgerald G, Ross RP (2008) Life under stress: the probiotic stress response and how it may be manipulated. Curr Pharm Des 14:1382–1399

    Article  CAS  Google Scholar 

  • Corthier G, Renault P (1999) Future directions for research on biotherapeutic agents: contribution of genetic approaches on lactic acid bacteria. In Elmer GW, McFarland L, Surawicz C (Eds.), Biotherapeutic agents and infectious diseases. Humana Press, Totowa, NJ, pp. 269–304

    Google Scholar 

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

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Derzelle S, Hallet B, Ferain T, Delcour J, Hols P (2002) Cold shock induction of the cspL gene in Lactobacillus plantarum involves transcriptional regulation. J Bacteriol 184:5518–5523

    Article  CAS  Google Scholar 

  • Derzelle S, Hallet B, Ferain T, Delcour J, Hols P (2003) Improved adaptation to cold shock, stationary-phase, and freezing stresses in Lactobacillus plantarum overproducing cold-shock proteins. Appl Environ Microbiol 69:4285–4290

    Article  CAS  Google Scholar 

  • Digel I, Kayser P, Artmann GM (2008) Molecular processes in biological thermosensation,J Biophys 2008:602870

    CAS  Google Scholar 

  • Dixon-Fyle SM, Caro L (1999) Characterization in vitro and in vivo of a new HU family protein from Streptococcus thermophilus ST11. Plasmid 42:159–173

    Article  CAS  Google Scholar 

  • Dorman CJ, Deighan P (2003) Regulation of gene expression by histone-like proteins in bacteria. Curr Opin Genet Dev 13:179–184

    Article  CAS  Google Scholar 

  • Dumont F, Marechal PA, Gervais P (2003) Influence of cooling rate on Saccharomyces cerevisiae destruction during freezing: unexpected viability at ultra-rapid cooling rates. Cryobiology 46:33–42

    Article  Google Scholar 

  • Dumont F, Marechal PA, Gervais P (2004) Cell size and water permeability as determining factors for cell viability after freezing at different cooling rates. Appl Env Microbiol 70:268–272

    Article  CAS  Google Scholar 

  • El-Sharoud WM (2005) Two-component signal transduction systems as key players in stress responses of lactic acid bacteria. Sci Prog 88:203–228

    Article  CAS  Google Scholar 

  • Eriksson S, Hurme R, Rhen M (2002) Low-temperature sensors in bacteria. Phil Trans R Soc Lond 357:887–893

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Feng W, Tejero R, Zimmerman DE, Inouye M, Montelione GT (1998) 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. Biochem 37:10881–10896

    Article  CAS  Google Scholar 

  • Fernandez Murga ML, Pesce de Ruiz Holgado A, Font de Valdez G (1998) Survival rate and enzyme activities of Lactobacillus acidophilus following frozen storage. Cryobiology 36:315–319

    Article  Google Scholar 

  • Fernandez Murga ML, Cabrera GM, De Valdez GF, Disalvo A, Seldes AM (2000) Influence of growth temperature on cryotolerance and lipid composition of Lactobacillus acidophilus. J Appl Microbiol 88:342–348

    Article  CAS  Google Scholar 

  • Fiocco D, Capozzi V, Goffin P, Hols P, Spano G (2007) Improved adaptation to heat, cold and solvent tolerance in Lactobacillus plantarum. Appl Microbiol Biotech 77:909–915

    Article  CAS  Google Scholar 

  • Fiocco D, Collins M, Muscariello L, Hols P, Kleerebezem M, Msadek T, Spano G (2009) The Lactobacillus plantarum ftsH gene is a novel member of the CtsR stress response regulon. J Bacteriol 191:1688–1694

    Article  CAS  Google Scholar 

  • Fonseca F, Béal C, Corrieu G (2001) Operating conditions that affect the resistance of lactic acid bacteria to freezing and frozen storage. Cryobiology 43:189–198

    Article  CAS  Google Scholar 

  • Fonseca F, Béal C, Mihoub F, Marin M, Corrieu G (2003) Improvement of cryopreservation of Lactobacillus delbrueckii subsp. bulgaricus CFL1 with additives displaying different protective effects. Int Dairy J 13:917–926

    Article  CAS  Google Scholar 

  • Foschino R, Fiori E, Galli A (1996) Survival and residual activity of Lactobacillus acidophilus frozen cultures under different conditions. J Dairy Res 63:295–303

    Article  CAS  Google Scholar 

  • Giuliodori AM, Gualerzi CO, Soto S, Vila J, Tavio MM (2005) Review on bacterial stress topics. Ann NY Acad Sci 1113:95–104

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gómez Zavaglia A, Disalvo EA, De Antoni GL (2000) Fatty acid composition and freeze-thaw resistance in lactobacilli. J Dairy Res 67:241–247

    Article  Google Scholar 

  • Gordon BR, Imperial R, Wang L, Navarre WW, Liu J (2008) Lsr2 of Mycobacterium represents a novel class of H-NS-like proteins. J Bacteriol 190:7052–7509

    Article  CAS  Google Scholar 

  • Graumann P, Marahiel MA (1997) Effects of heterologous expression of CspB, the major cold shock protein of Bacillus subtilis, on protein synthesis in E. coli. Mol Gen Genet 253:745–752

    Article  CAS  Google Scholar 

  • Graumann P, Marahiel MA (1998) A superfamily of proteins that contain the cold-shock domain. Trends Biochem Sci 23:286–290

    Article  CAS  Google Scholar 

  • Graumann PL, Marahiel MA (1999) Cold shock response in Bacillus subtilis. J Mol Microbiol Biotechnol 1:203–209

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Graumann P, Wendrich TM, Weber MHW, Schröder K, Marahiel MA (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

    Article  CAS  Google Scholar 

  • Gualerzi CO, Giuliodori AM, Pon CL (2003) Transcriptional and post-transcriptional control of cold-shock genes. J Mol Biol 331:527–539

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hayashi K, Kojima C (2008) pCold-GST vector: a novel cold-shock vector containing GST tag for soluble protein production. Protein Expr Purif 62:120–127

    Article  CAS  Google Scholar 

  • Hecker M, Schumann W, Volker U (1996) Heat shock and general stress response in Bacillus subtilis. Mol Microbiol 19:417–428

    Article  CAS  Google Scholar 

  • Hunger K, Beckering CL, Marahiel MA (2004) Genetic evidence for the temperature-sensing ability of the membrane domain of the Bacillus subtilis histidine kinase DesK. FEMS Microbiol Lett 230:41–46

    Article  CAS  Google Scholar 

  • Jin S, Song YN, Deng WY, Gordon MP, Nester EW (1993) The regulatory VirA protein of Agrobacterium tumefaciens does not function at elevated temperatures. J Bacteriol 175:6830–6835

    CAS  Google Scholar 

  • Jones PG, Van Bogelen RA, Neidhardt FC (1987) Induction of proteins in response to low temperature in Escherichia coli. J Bacteriol 169:2092–2095

    CAS  Google Scholar 

  • Jones PG, Krah R, Tafuri SR, Wolffe AP (1992a) DNA gyrase, CS7.4, and the cold shock response in Escherichia coli. J Bacteriol 174:5798–5802

    CAS  Google Scholar 

  • Jones PG, Cashel M, Glaser G, Neidhardt FC (1992b) Function of a relaxed-like state following temperature downshifts in Escherichia coli. J Bacteriol 174:3903–3914

    CAS  Google Scholar 

  • Kaufman-Szymczyk A, Wojtasik A, Parniewsky P, Bialkowska A, Tkaczuk K, Turkiewicz M (2009) Identification of the csp gene and molecular modelling of the CspA-like protein from antarctic soil-dwelling psychrotrophic bacterium Psychrobacter sp. B6. Acta Biochim Polonica 56:63–69

    CAS  Google Scholar 

  • Keskinen LA, Todd EC, Ryser ET (2008) Impact of bacterial stress and biofilm-forming ability on transfer of surface-dried Listeria monocytogenes during slicing of delicatessen meats. Int J Food Microbiol 127:298–304

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kives J, Guadarrama D, Orgaz B, Rivera-Sen A, Vazquez J, San Jose C (2005) Interactions in biofilms of Lactococcus lactis ssp. cremoris and Pseudomonas fluorescens cultured in cold UHT Milk. J Dairy Sci 88:4165–4171

    Article  CAS  Google Scholar 

  • Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, Leer R, Tarchini R, Peters SA, Sandbrink HM, Fiers MW, Stiekema W, Lankhorst RM, Bron PA, Hoffer SM, Groot MN, Kerkhoven R, de Vries M, Ursing B, de Vos WM, Siezen RJ (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci USA 100:1990–1995

    Article  CAS  Google Scholar 

  • Klinkert B, Narberhaus F (2009) Microbial thermosensors. Cell Mol Life Sci 66:2661–2676

    Article  CAS  Google Scholar 

  • Kremer W, Schuler B, Harrieder S, Geyer M, Gronwald W, Welker C, Jaenicke R, Kalbitzer HR (2001) Solution NMR structure of the cold-shock protein from the hyperthermophilic bacterium Thermotoga maritima. Eur J Biochem 268:2527–2539

    Article  CAS  Google Scholar 

  • Lee HS, Berger DK, Kustu S (1993). Activity of purified NIFA, a transcriptional activator of nitrogen fixation genes. Proc Natl Acad Sci USA 90:2266–2270

    Article  CAS  Google Scholar 

  • Lee K (2004) Cold shock response in Lactococcus lactis ssp. diacetylactis: a comparison of the protection generated by brief pre-treatment at less severe temperatures. Process Biochem 39:2233–2239

    Article  CAS  Google Scholar 

  • Li C, Jia-Liang Z, Yu-Tang W, Xu H, Ning L (2009) Synthesis of cyclopropane fatty acid and its effect on freeze-drying survival of Lactobacillus bulgaricus L2 at different growth conditions. World J Microbiol Biotechnol 25:1659–1665

    Article  CAS  Google Scholar 

  • Liu D, Yumoto H, Murakami K, Hirota K, Ono T, Nagamune H, Kayama S, Matsuo T, Miyake Y (2008) The essentiality and involvement of Streptococcus intermedius histone-like DNA-binding protein in bacterial viability and normal growth. Mol Microbiol 68:1268–1282

    Article  CAS  Google Scholar 

  • Margesin R, Neuner G, Storey KB (2007) Cold-loving microbes, plants, and animals-fundamental and applied aspects. Naturwissenschaften 94:77–99

    Article  CAS  Google Scholar 

  • Mitta M, Fang L, Inouye M (1997) Deletion analysis of cspA of Escherichia coli: requirement of the AT-rich UP element for cspA transcription and the downstream box in the coding region for its cold shock induction. Mol Microbiol 26:321–335

    Article  CAS  Google Scholar 

  • Molenaar D, Bringel F, Schuren FH, de Vos WM, Siezen RJ, Kleerebezem M (2005) Exploring Lactobacillus plantarum genome diversity by using microarrays. Microbiology 187:6119–6127

    CAS  Google Scholar 

  • Monnet C, Béal C, Corrieu G (2003) Improvement of the resistance of Lactobacillus delbrueckii ssp. bulgaricus to freezing by natural selection. J Dairy Sci 86:3048–3053

    Article  CAS  Google Scholar 

  • Mueller U, Perl D, Schmid FX, Heinemann U (2000) Thermal stability and atomic-resolution crystal structure of the Bacillus caldolyticus cold shock protein. J Mol Biol 297:975–988

    Article  CAS  Google Scholar 

  • Muldrew K, McGann LE (1990) Mechanisms of intracellular ice formation. Biophys J 57:525–532

    Article  CAS  Google Scholar 

  • Nierlich DP, Murakawa GJ (1996) The decay of bacterial messenger RNA. Prog Nucleic Acid Res Mol Biol 52:153–216

    Article  CAS  Google Scholar 

  • Ouvry A, Wache Y, Tourdot-Maréchal R, Diviès C, Cachon R (2002) Effects of oxidoreduction potential combined with acetic acid, NaCl and temperature on the growth, acidification, and membrane properties of Lactobacillus plantarum. FEMS Microbiol Lett 214:257–261

    Article  CAS  Google Scholar 

  • Palmfeldt J, Hahn-Hagerdal B (2000) Influence of culture pH on survival of Lactobacillus reuteri subjected to freeze-drying. Int J Food Microbiol 55:235–238

    Article  CAS  Google Scholar 

  • Panoff JM, Thammavongs B, Laplace J, Hartke A, Boutibonnes P, Auffray Y (1995) Cryotolerance and cold adaptation in Lactococcus lactis subsp. lactis IL 1403. Cryobiology 32:516–520

    Article  Google Scholar 

  • Panoff JM, Bouachanh T, Micheline G, Boutibonnes P (1998) Cold stress response in mesophilic bacteria. Cryobiology 36:75–83

    Article  CAS  Google Scholar 

  • Panoff JM, Bouachanh T, Micheline G (2000) Cryoprotectants lead to phenotypic adaptation to freeze–thaw in Lactobacillus delbrueckii ssp. bulgaricus CIP 101027T. Cryobiology 40:264–269

    Article  CAS  Google Scholar 

  • Phadtare S (2004) Recent developments in bacterial cold-shock response. Curr Issues Mol Biol 6:125–136

    CAS  Google Scholar 

  • Phadtare S, Hwang J, Severinov K, Inouye M (2003) CspB and CspL, thermostable cold-shock proteins from Thermotoga maritima. Genes Cells 8:801–810

    Article  CAS  Google Scholar 

  • Qing G, Ma LC, Khorchid A, Swapna GV, Mal TK, Takayama MM, Xia B, Phadtare S, Ke H, Acton T, Montelione GT, Ikura M, Inouye M (2004) Cold-shock induced high-yield protein production in Escherichia coli. Nat Biotechnol 22:877–882

    Article  CAS  Google Scholar 

  • Rivals JP, Beal C, Thammavongs B, Gueguen M, Panoff JM (2007) Cryotolerance of Lactobacillus delbrueckii subsp. bulgaricus CFL1 is modified by acquisition of antibiotic resistance. Cryobiology 55:19–26

    Article  CAS  Google Scholar 

  • Rosen R, Ron EZ (2002) Proteome analysis in the study of the bacterial heat shock response. Mass Spectr Rev 21:244–265

    Article  CAS  Google Scholar 

  • Russell NJ, Evans RI, ter Steeg PF, Hellemons J, Verheul A, Abee T (1995) Membranes as a target for stress adaptation. Int J Food Microbiol 28:255–261

    Article  CAS  Google Scholar 

  • Saarela M, Virkajärki I, Alakomi HL, Mattila-Sandholm T, Vaari A, Suomalainen T, Mättö J (2005) Influence of fermentation time, cryoprotectant and neutralization of cell concentrate on freeze-drying survival, storage stability, and acid and bile exposure of Bifidobacterium animalis ssp. lactis cells produced without milk-based ingredients. J Appl Microbiol 99:1330–1339

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schindelin H, Marahiel MA, Heinemann U (1993) Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein. Nature 364:164–168

    Article  CAS  Google Scholar 

  • Schumann W (2009) Temperature sensors of eubacteria. Adv Appl Microbiol 67:213–256

    Article  CAS  Google Scholar 

  • Siaterlis A,  Deepika G,  Charalampopoulos D (2009) Effect of culture medium and cryoprotectants on the growth and survival of probiotic lactobacilli during freeze drying. Lett Appl Microbiol 48:295–301

    Article  CAS  Google Scholar 

  • Skinner MM, Trempy JE (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

    Article  CAS  Google Scholar 

  • Sledjeski DD, Gupta A, Gottesman S (1996) The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J 15:3993–4000

    CAS  Google Scholar 

  • Smirnova AV, Braun Y, Ullrich MS (2008) Site-directed mutagenesis of the temperature-sensing histidine protein kinase CorS from Pseudomonas syringae. FEMS Microbiol Lett 283:231–238

    Article  CAS  Google Scholar 

  • Spano G, Massa S (2006) Environmental stress response in wine lactic acid bacteria: beyond Bacillus subtilis. Crit Rev Microbiol 32:77–86

    Article  CAS  Google Scholar 

  • Spano G, Capozzi V, Vernile A, Massa S (2004) Cloning, molecular characterization and expression analysis of two small heat shock genes isolated from wine Lactobacillus plantarum. J Appl Microbiol 97:774–782

    Article  CAS  Google Scholar 

  • Spano G, Beneduce L, Perrotta C, Massa S (2005) Cloning and characterization of the hsp 18.55 gene, a new member of the small heat shock genes family isolated from wine Lactobacillus plantarum. Res Microbiol 156:219–224

    CAS  Google Scholar 

  • Stead D, Park SF (2000) Roles of Fe superoxide dismutase and catalase in resistance of Campylobacter coli to freeze–thaw stress. Appl Environ Microbiol 66:3110–3112

    Article  CAS  Google Scholar 

  • Streit F, Corrieu G, Béal C (2007) Acidification of fermented broth improves cryotolerance of Lactobacillus delbrueckii subsp. bulgaricus CFL1. J Biotech 128:659–667

    Article  CAS  Google Scholar 

  • Streit F, Delettre J, Corrieu G, Béal C (2008) Acid adaptation of Lactobacillus delbrueckii subsp. bulgaricus induces physiological responses at membrane and cytosolic levels that improves cryotolerance. J Appl Microbiol 105:1071–1080

    Article  CAS  Google Scholar 

  • Suutari M, Laakso S (1992) Changes in fatty acid branching and unsaturation of Streptomyces griseus and Brevibacterium fermentans as a response to growth temperature. Appl Environ Microbiol 58:2338–2340

    CAS  Google Scholar 

  • Tendeng C, Bertin PN (2003) H-NS in Gram-negative bacteria: a family of multifaceted proteins. Trends Microbiol 11:511–518

    Article  CAS  Google Scholar 

  • van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E (2002) Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek 82:187–216

    Article  Google Scholar 

  • Varcamonti M, Arsenijevic S, Martirani L, Fusco D, Naclerio G, De Felice M (2006) Expression of the heat shock gene clpL of Streptococcus thermophilus is induced by both heat and cold shock. Microbial Cells Factories 5:1–6

    Article  CAS  Google Scholar 

  • Vorob’eva LI (2004) Stressors, stress reactions, and survival of bacteria (a review). Prikl Biokhim Mikrobiol 40:261–269

    Google Scholar 

  • Walker DC, Girgis HS, Klaenhammer TR (1999) The groESL chaperone operon of Lactobacillus johnsonii. Appl Environ Microbiol 65:3033–3041

    CAS  Google Scholar 

  • Wang Y, Corrieu G, Béal C (2005a) Fermentation pH and temperature influence the cryotolerance of Lactobacillus acidophilus RD758. J Dairy Sci 88:21–29

    Article  CAS  Google Scholar 

  • Wang Y, Delettre J, Guillot A, Corrieu G, Béal C (2005b) Influence of cooling temperature and duration on cold adaptation of Lactobacillus acidophilus RD758. Cryobiology 50:294– 307

    Article  CAS  Google Scholar 

  • Weber MH, Marahiel MA (2002) Coping with the cold: the cold shock response in the Gram-positive soil bacterium Bacillus subtilis. Philos Trans R Soc Lond B Biol Sci 357:895–907

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Wouters JA, Jeynov B, Rombouts FM, de Vos WM, Kuipers OP, Abee T (1999a) Analysis of the role of 7 kDa cold- shock proteins of Lactococcus lactis MG1363 in cryoprotection. Microbiology 145:3185–3194

    CAS  Google Scholar 

  • Wouters JA, Rombouts FM, Kuipers OP, De Vos WM, Abee T (2000) The role of cold-shock proteins in low-temperature adaptation of food-related bacteria. System Appl Microbiol 23:165–173

    Google Scholar 

  • Zangrossi S, Briani F, Ghisotti D, Regonesi ME, Tortora P, Deho G (2000) Transcriptional and post-transcriptional control of polynucleotide phosphorylase during cold acclimation in Escherichia coli. Mol Microbiol 36:1470–1480

    Article  CAS  Google Scholar 

  • Zeeb M, Klaas EAM, Weininger U, Löw C, Sticht H, Balbach J (2006) Recognition of T-rich single-stranded DNA by the cold shock protein Bs-CspB in solution. Nucleic Acids Res 34:4561–4571

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Giuseppe Spano .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Capozzi, V., Fiocco, D., Spano, G. (2011). Responses of Lactic Acid Bacteria to Cold Stress. In: Tsakalidou, E., Papadimitriou, K. (eds) Stress Responses of Lactic Acid Bacteria. Food Microbiology and Food Safety. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-92771-8_5

Download citation

Publish with us

Policies and ethics