Skip to main content
SpringerLink
Log in
Book cover

Stress Responses of Lactic Acid Bacteria pp 219–249Cite as

Stress Responses of Lactobacilli

  • Chapter
  • First Online:

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

Abstract

Environmental stress responses in Lactobacillus are reviewed in this chapter. Comparative genome analysis of the Lactobacillus species indicated that the combination of gene gain and gene loss occurred during environmental adaptation. However, the ability of the Lactobacillus species to adapt to different environments is variable. The physiological and molecular mechanisms of responses to heat, cold, acid, osmotic, oxidative, high pressure, starvation, and quorum-sensing (QS) stresses are described. The mechanisms of stress resistance in lactobacilli are based upon the induction of a specific set of proteins found after exposure to sublethal specific stress (specific response) or after exposure to other types of environmental stress (generic response). Other mechanisms of stress responses are involved, such as (1) the proportion of shorter and/or unsaturated fatty acids in membrane lipids, (2) the intracellular level of compatible solutes, (3) the F0F1-ATPase proton pumps, (4) the amino acid decarboxylation/catabolism, and (5) the small signaling hormone-like molecules. Molecular mechanisms of stress responses in lactobacilli and other bacteria are compared. Specific examples of the repercussions of these effects in food processing are given.

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

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

Learn about institutional subscriptions

References

  • Abe K, Hayashi H, Maloney PC (1996) Exchange of aspartate and alanine. J Biol Chem 271:3079–3084

    Article  CAS  Google Scholar 

  • Altermann E, Russell WM, Azcarate-Peril MA, Barrangou R, Buck BL, McAuliffe O, Souther N, Dobson A, Duong T, Callanan M, Lick S, Hamrick A, Cano R, Klaenhammer TR (2005) Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc Natl Acad Sci USA 102:3906–3912

    Article  CAS  Google Scholar 

  • Amanatidou A, Bennik MHJ, Gorris LGM, Smid EJ (2001) Superoxide dismutase plays an important role in the survival of Lactobacillus sake upon exposure to elevated oxygen. Arch Microbiol 176:79–88

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Arena ME, Saguir FM, Manca de Nadra MC (1999) Arginine dihydrolase pathway in Lactobacillus plantarum from orange. Int J Food Microbiol 47:203–209

    Article  CAS  Google Scholar 

  • Azcarate-Peril MA, Altermann E, Hoover-Fitzula RL, Cano RJ, Klaenhammer TR (2004) Identification and inactivation of genetic loci involved with Lactobacillus acidophilus acid tolerance. Appl Environ Microbiol 70:5315–5322

    Article  CAS  Google Scholar 

  • Azcarate-Peril MA, McAuliffe O, Altermann E, Lick S, Russell WM, Klaenhammer TR (2005) Microarray analysis of a two-component regulatory system involved in acid resistance and proteolytic activity in Lactobacillus acidophilus. Appl Environ Microbiol 71:5794–5804

    Article  CAS  Google Scholar 

  • Bâati L, Fabre-Gea C, Auriol D, Blanc PJ (2000) Development of bioactive food packaging materials using immobilised bacteriocins Lacticin 3147 and Nisaplin®. Int J Food Microbiol 59:241–247

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bass S, Gu Q, Christen A (1996) Multicopy suppressors of prc mutant Escherichia coli include two HtrA (DegP) protease homologs (HhoAB), DksA, and a truncated R1pA. J Bacteriol 178:1154–1161

    CAS  Google Scholar 

  • Bender GR, Marquis, RE (1987) Membrane ATPases and acid tolerance of Actinomyces viscosus and Lactobacillus casei. Appl Environ Microbiol 53:2124–2128

    CAS  Google Scholar 

  • Broadbent JR, Oberg JC, Wang H, Wie L (1997) Attributes of the heat shock response in three species of dairy Lactobacillus. Syst Appl Microbiol 20:12–19

    Google Scholar 

  • Broadbent JR, Oberg CJ, Wie L (1998) Characterization of the Lactobacillus helveticus groESL operon. Res Microbiol 149:247–253

    Article  CAS  Google Scholar 

  • Cai H, R Thompson, Budinich MF, Broadbent JR, Steele JL (2009) Genome sequence and comparative genome analysis of Lactobacillus casei: insights into their niche-associated evolution. Gen Biol Evol 9:239–257

    Google Scholar 

  • Callanan M, Kaleta P, O’Callaghan J, O’Sullivan O, Jordan K, McAuliffe O, Sangrador-Vegas A, Slattery L, Fitzgerald, Beresford T, Ross RP (2008) Genome sequence of Lactobacillus helveticus, an organism distinguished by selective gene loss and insertion sequence element expansion. J Bacteriol 190:727–735

    Article  CAS  Google Scholar 

  • Cappa F, Cattivelli D, Cocconcelli PS (2005) The uvrA gene is involved in oxidative and acid stress responses in Lactobacillus helveticus CNBL1156. Res Microbiol 156:1039–1047

    Article  CAS  Google Scholar 

  • Castaldo C, Siciliano RA, Muscariello L, Marasco R, Sacco M (2006) CcpA affects expression of the groESL and dnaK operons in Lactobacillus plantarum. Microb Cell Fact 5:35

    Article  CAS  Google Scholar 

  • Castro HP, Teixeira PM, Kirby R (1997) Evidence of membrane damage in Lactobacillus bulgaricus following freeze drying. J Appl Microbiol 82:87–94

    Article  CAS  Google Scholar 

  • Chaillou S, Champomier-Vergès MC, Cornet M, Crutz-Le Coq AM, Dudez AM, Martin V, Beaufils S, Darbon-Rongere E, Bossy R, Loux V, Zagorec M (2005) The complete genome sequence of the meat-borne lactic acid bacterium Lactobacillus sakei 23 K. Nat Biotechnol 23:1527–1533

    Article  CAS  Google Scholar 

  • Champomier Vergès MC, Zúňiga M, Morel-Deville F, Pèrez-Martinez G, Zagorec M, Ehrlich SD (1999) Relationships between arginine degradation, pH and survival in Lactobacillus sakei.  FEMS Microbiol Lett 180:297–304

    Article  Google Scholar 

  • Chatterji D, Ojha A K (2001) Revisiting the stringent response, ppGpp and starvation signaling. Curr Opinion Microbiol 4(2):160–165

    Article  CAS  Google Scholar 

  • Chou LS, Weimer B (1999) Isolation and characterization of acid- and bile-tolerant isolates from strains of Lactobacillus acidophilus. J Dairy Sci 82:23–31

    Article  CAS  Google Scholar 

  • Cohen DPA, Renes J, Bouwman FG, Zoetendal1 EG, Mariman E, de Vos WM, Vaughan EE (2006) Proteomic analysis of log to stationary growth phase Lactobacillus plantarum cells and a 2-DE database. Proteomics 6:6485–6493

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Corcoran BM, Ross RP, Fitzgerald GF, Dockery P, Stanton C (2006) Enhanced survival of GroESL-overproducing Lactobacillus paracasei NFBC 338 under stressful conditions induced by drying. Appl Environ Microbiol 72:5104–5107

    Article  CAS  Google Scholar 

  • Cotter PD, Hill C (2003) Surviving the acid test: responses of Gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67:429–453

    Article  CAS  Google Scholar 

  • De Angelis M, Gobbetti M (1999) Lactobacillus sanfranciscensis CB1: manganese, oxygen, superoxide dismutase and metabolism. Appl Microbiol Biotechnol 51:358–363

    Article  Google Scholar 

  • De Angelis M, Gobbetti M (2004) Environmental stress responses in Lactobacillus: a review. Proteomics 4:106–122

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • De Angelis M, Mariotti L, Rossi J, Servili M, Fox P, Rollan G, Gobbetti M (2002) Arginine catabolism by sourdough lactic acid bacteria: purification and characterization of the arginine deiminase pathway enzymes from Lactobacillus sanfranciscensis CB1. Appl Environ Microbiol 68:6193–6201

    Article  CAS  Google Scholar 

  • De Angelis M, Di Cagno R, Huet C, Crecchio C, Fox PF, Gobbetti M (2004) Heat shock response in Lactobacillus plantarum. Appl Environ Microbiol 70:1336–1346

    Article  CAS  Google Scholar 

  • Derré 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

    Article  Google Scholar 

  • Derzelle S, Hallet B, Francis KP, 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

    Article  CAS  Google Scholar 

  • Desmond C, Stanton C, Fitzgerald GF, Collins K, Ross RP (2001) Environmental adaptation of probiotic lactobacilli towards improvement of performance during spray drying. Int Dairy J 11:801–808

    Article  Google Scholar 

  • Di Cagno R, De Angelis M, Limitone A, Fox PF, Gobbetti M (2006) Response of Lactobacillus helveticus PR4 to heat stress during propagation in cheese whey with a gradient of decreasing temperatures. Appl Environ Microbiol 72:4503–4514

    Article  CAS  Google Scholar 

  • Di Cagno R, De Angelis M, Limitone A, Minervini F, Simonetti C, Buchin S, Gobbetti M (2007) Cell-cell communication in sourdough lactic acid bacteria: a proteomic study in Lactobacillus sanfranciscensis CB1. Proteomics 7:2430–2446

    Article  Google Scholar 

  • Di Cagno R, De Angelis M, Coda R, Minervini F, Gobbetti M (2009) Molecular adaptation of sourdough Lactobacillus plantarum DC400 under co-cultivation with other lactobacilli. Microbiol Res 160:358 –366

    Article  CAS  Google Scholar 

  • Di Cagno R, De Angelis M, Calasso M, Vicentini O, Vernocchi P, Ndagijimana M, De Vincenzi M, Dessì M, Guerzoni ME, Gobbetti M (2010) Quorum sensing in sourdough Lactobacillus plantarum DC400: induction of plantaricin A (PlnA) under co-cultivation with other lactic acid bacteria and effect of PlnA on bacterial and Caco-2 cells. Proteomics, in press

    Google Scholar 

  • Drews O, Weiss W, Reil G, Parlar H, Wait R, Görg A (2002) High pressure effects step-wise altered protein expression in Lactobacillus sanfranciscensis. Proteomics 2:765–774

    Article  CAS  Google Scholar 

  • Elli M, Morelli L, Zink R (2002) In: Book of Abstracts, “Seventh Symposium on Lactic Acid Bacteria—genetics, metabolism and applications,” FEMS Netherlands, p. G9

    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 Biotechnol 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 

  • Foster JW, Hall HK (1991) Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J Bacteriol 173:5129–5135

    CAS  Google Scholar 

  • Francis KP, Stewart GSAB (1997) Detection and speciation of bacteria through PCR using universal major cold-shock protein primer oligomers. J Ind Microbiol Biotechnol 19:286–293

    Article  CAS  Google Scholar 

  • Gaenzle MG, Schwab C (2009) Ecology of exopolysaccharide formation by lactic acid bacteria: sucrose utilisation, stress tolerance, and biofilm formation. In: Ulrich M (Ed.), Bacterial polysaccharides—current innovation and trends. Horizon Press

    Google Scholar 

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

    CAS  Google Scholar 

  • Glaasker E, Tjan FSB, Tergesteeg PF, Konings WN, Poolman B (1998) Physiological response of Lactobacillus plantarum to salt and nonelectrolyte stress. J Bacteriol 180:4718–4723

    CAS  Google Scholar 

  • Gobbetti M (1998) The sourdough microflora: interactions of lactic acid bacteria and yeasts. Trends Food Sci Technol 9:267–274

    Article  CAS  Google Scholar 

  • Gobbetti M, De Angelis M, Di Cagno R, Minervini F, Limitone A (2007) Cell cell communication in food related bacteria. Int J Food Microbiol 120:34–45

    Article  CAS  Google Scholar 

  • Goh Y, Klaenhammer TR (2009) Genomic features of Lactobacillus species. Front Biosci 14:1362–1386

    Article  CAS  Google Scholar 

  • Götz F, Sedewitz B, Elstner EF (1980) Oxygen utilization by Lactobacillus plantarum. Arch Microbiol 125:209–214

    Article  Google Scholar 

  • Gouesbert G, Jan G, Boyaval P (2001) Lactobacillus delbrueckii ssp. bulgaricus thermotolerance. Lait 81:301–309

    Article  Google Scholar 

  • Groot MN, Klaassens E, de Vos WM, Delcour J, Hols P, Kleerebezem M (2005) Genome-based in silico detection of putative manganese transport systems in Lactobacillus plantarum and their genetic analysis. Microbiology 151:1229–1238

    Article  CAS  Google Scholar 

  • Guerzoni ME, Lanciotti R, Cocconcelli PS (2001) Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. Microbiology 147:2255–2264

    CAS  Google Scholar 

  • Guerzoni ME, Vernocchi P, Ndagijimana M, Giannotti A, Lanciotti R (2007) Generation of aroma compounds in sourdough: effects of stress exposure and lactobacilli–yeasts interactions. Food Microbiol 24:139–148

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Hong SI, Kim YJ, Pyun YR (1999) Acid tolerance of Lactobacillus plantarum from Kimchi. Food Sci Technol Lebensm Wiss Technol 32:142–148

    Article  CAS  Google Scholar 

  • Hörmann S, Scheyhing C, Behr J, Pavlovic M, Ehrmann M, Vogel RF (2006) Comparative proteome approach to characterize the high-pressure stress response of Lactobacillus sanfranciscensis DSM 20451 T. Proteomics 6:1878–1885

    Article  CAS  Google Scholar 

  • Horn G, Hofweber R, Kremer W, Kalbitzer HR (2007) Structure and function of bacterial cold shock proteins. Cell Mol Life Sci 64:1457–1470

    Article  CAS  Google Scholar 

  • Hussain MA, Knight MI, Britz ML (2009) Proteomic analysis of lactose-starved Lactobacillus casei. J Appl Microbiol 106(3):764–773

    Article  CAS  Google Scholar 

  • Hutkins RW, Nannen NL (1993) pH homeostasis in lactic acid bacteria. J Dairy Sci 76:2354–2365

    Article  CAS  Google Scholar 

  • Ito K, Akiyama Y (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59:211–231

    Article  CAS  Google Scholar 

  • Jänsch A, Korakli M, Vogel RF, Gänzle MG (2007) Glutathione reductase from Lactobacillus sanfranciscensis DSM20451T: contribution to oxygen tolerance and thiol exchange reactions in wheat sourdoughs. Appl Environ Microbiol 73:4469–4476

    Article  CAS  Google Scholar 

  • Jofré A, Champomier-Vergès SM, Anglade P, Baraige F, Martìn B, Garriga M, Zagorec M, Aymerich T (2007) Protein synthesis in lactic acid and pathogenic bacteria during recovery from a high pressure treatment. Res Microbiol 158:512–520

    Article  CAS  Google Scholar 

  • Jordan S, Hutchings MI, Mascher T (2008) Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol Rev 32:107–146

    Article  CAS  Google Scholar 

  • Katsaros GI, Giannoglou MN, Taoukis PS (2009) Kinetic study of the combined effect of high hydrostatic pressure and temperature on the activity of Lactobacillus delbrueckii ssp. bulgaricus aminopeptidases. J Food Sci 74:E219–E225

    Article  CAS  Google Scholar 

  • Kilimann KV, Doster W, Vogel RF, Hartmann C, Gänzle MG (2006a) Protection by sucrose against heat-induced lethal and sublethal injury of Lactococcus lactis: an FT-IR study. Biochim Biophys Acta 1764:1188–1197

    CAS  Google Scholar 

  • Kilimann KV, Hartmann C, Delgado A, Vogel RF, Gänzle MG (2006b) Combined high pressure and temperature induced lethal and sublethal injury of Lactococcus lactis—application of multivariate statistical analysis. Int J Food Microbiol 109:25–33

    Article  CAS  Google Scholar 

  • Kim SW, 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 

  • Kim WS, Perl L, Park JH, Tandianus JE, Dunn NW (2001) Assessment of stress response of the probiotic Lactobacillus acidophilus. Curr Microbiol 43:346–350

    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 

  • Knauf HJ, Vogel RF, Hammes WP (1992) Cloning, sequence, and phenotypic expression of katA, which encodes the catalase of Lactobacillus sake LTH677. Appl Environ Microbiol 58:832–839

    CAS  Google Scholar 

  • Korakli M, Gänzle MG, Knorr R, Frank M, Rossmann A, Vogel RF (2002) Metabolism of Lactobacillus sanfranciscensis under high-pressure: investigations using stable carbon isotopes. In: Hayashi R (Ed.), Trends in high pressure bioscience and biotechnology. Elsevier, Amsterdam, pp. 287–294

    Chapter  Google Scholar 

  • Laplace JM, Sauvageot N, Harke A, Auffray Y (1999) Characterization of Lactobacillus collinoides response to heat, acid and ethanol treatments. Appl Microbiol Biotechnol 51:659–663

    Article  CAS  Google Scholar 

  • Lee K, Lee HG, Pi KB, Choi YJ (2008) The effect of low pH on protein expression by the probiotic bacterium Lactobacillus reuteri. Proteomics 8:1624–1630

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lim EM, Smokvina T, Chervaux C, Ehrlich SD, Maguin E (2002) In: Book of Abstracts, “Seventh Symposium on Lactic Acid Bacteria—genetics, metabolism and applications,” FEMS Netherlands, p. G85

    Google Scholar 

  • Lorca GL, Raya RR, Taranto MP, Font de Valdez G (1998) Adaptative acid tolerance response in Lactobacillus acidophilus. Biotechnol Lett 20:239–241

    Article  CAS  Google Scholar 

  • Lorca GL, Font de Valdez GF (1999) Effect of suboptimal growth temperature and growth phase on resistance of Lactobacillus acidophilus to environmental stress. Cryobiology 39:144–149

    Article  CAS  Google Scholar 

  • Lorca GL, Font de Valdez G (2001) Acid tolerance mediated by membrane ATPases in Lactobacillus acidophilus. Curr Microbiol 42:21–25

    Article  CAS  Google Scholar 

  • Marceau A, Zagorec M, Champonier-Vergès MC (2002) In: Book of Abstracts, “Seventh Symposium on Lactic Acid Bacteria—genetics, metabolism and applications,” FEMS Netherlands, p. G62

    Google Scholar 

  • Marquis RE, Mèra T, Bender GR, Murray DR, Pesce de Ruiz Holgado A (1987) Arginine deiminase system and bacterial adaptation to acid environments. Appl Environ Microbiol 53:198–200

    CAS  Google Scholar 

  • Martinac B, Adler J, Kung C (1990) Mechanosensitive ion channels of E. coli activated by amphipaths. Nature 348:261–263

    Article  CAS  Google Scholar 

  • Marty-Teysset C, De La Torre F, Garel JR (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

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Miyakawa H, Anjitsu K, Ishibashi N, Shimamura S (1994) Effects of pressure on enzyme activities of Lactobacillus helveticus LHE-511. Biosci Biotech Biochem 58:606–607

    Article  CAS  Google Scholar 

  • Molenaar D, Bosscher JS, Ten Brink B, Driessen AJM, Konings WN (1993) Generation of a proton motive force by histidine decarboxylation and electrogenic histidine/histamine antiport in Lactobacillus buchneri. J Bacteriol 175:2864–2870

    CAS  Google Scholar 

  • Moslehi-Jenabian S, Gori K, Jespersen L (2009) AI-2 signalling is induced by acidic shock in probiotic strains of Lactobacillus spp. Int J Food Microbiol 135:295–302

    Article  CAS  Google Scholar 

  • Nannen NL, Hutkins RW (1991) Proton-translocating adenosine triphosphatase activity in lactic acid bacterial. J Dairy Sci 74:747–751

    Article  CAS  Google Scholar 

  • Narberhaus F (2002) α-Crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66:64–93

    Article  CAS  Google Scholar 

  • Nousiainen LL, Savijoki K, Palva A, Varmanen P (2002) In: Book of Abstracts, “Seventh Symposium on Lactic Acid Bacteria—genetics, metabolism and applications,” FEMS, Netherlands, p. G44

    Google Scholar 

  • Pallen MJ, Wren BW (1997) The HtrA family of serine proteases. Mol Microbiol 26:209–221

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pavlovic M, Hörmann S, Vogel RF, Ehrmann MA (2005) Transcriptional response reveals translation machinery as target for high pressure in Lactobacillus sanfranciscensis. Arch Microbiol 184:11–17

    Article  CAS  Google Scholar 

  • Pavlovic M, Hörmann S, Vogel RF, Ehrmann MA (2008) Characterisation of a piezotolerant mutant of Lactobacillus sanfranciscensis. Z Naturforsch 63b:791–797

    Google Scholar 

  • Pfeiler EA, Azcarate-Peril MA, Klaenhammer TR (2007) Characterization of a novel bile-inducible operon encoding a two-component regulatory system in Lactobacillus acidophilus. J Bacteriol 189:4624–4634

    Article  CAS  Google Scholar 

  • Phadtare S, Yamanata K, Inouye M (2000) In: Stortz G, Hengge-Aronis R (Eds.), Bacterial stress response, ASM Press, Washinngton, DC, pp. 33–45

    Google Scholar 

  • Pieterse B, Leer RJ, Schuren FHJ, van der Werf M (2005) Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. Microbiology 151:3881–3894

    Article  CAS  Google Scholar 

  • Pridmore RD, Berger B, Desiere F, Vilanova D, Barretto C, Pittet AC, Zwahlen MC, Rouvet M, Altermann E, Barrangou R, Mollet B, Mercenier A, Klaenhammer T, Arigoni F, Schell MA (2004) The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc Natl Acad Sci USA 101:2512–2517

    Article  CAS  Google Scholar 

  • Rizzello CG, Cassone A, Di Cagno R, Gobbetti M (2008) Synthesis of angiotensin I-converting enzyme (ACE)-inhibitory peptides and g-aminobutyric acid (GABA) during sourdough fermentation by selected lactic acid bacteria. J Agric Food Chem 56:6936–6943

    Article  CAS  Google Scholar 

  • Rochat T, Gratadoux JJ, Gruss A, Corthier G, Maguin E, Langella P, van de Guchte M (2006) Production of a heterologous nonheme catalase by Lactobacillus casei: an efficient tool for removal of H2O2 and protection of Lactobacillus bulgaricus from oxidative stress in milk. Appl Environ Microbiol 72:5143–5149

    Article  CAS  Google Scholar 

  • Ruas-Madiedo P, Hugenholtz J, Zoon P (2000) An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. Int Dairy J 12:163–171

    Article  Google Scholar 

  • Russel NJ, Fukanage M (1990) A comparison of thermal adaptation of membrane lipids in psychrophilic and thermo-philic bacteria. FEMS Microbiol Rev 75:171–182

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Scheyhing CH, Hörmann S, Ehrmann MA, Vogel RF (2004) Barotolerance is inducible by preincubation under hydrostatic pressure, cold-, osmotic- and acid-stress conditions in Lactobacillus sanfranciscensis DSM20451T. Lett Appl Microbiol 39:284–289

    Article  CAS  Google Scholar 

  • Schmidt G, Hertel C, Hammes WP (1999) Characterisation of the dnaK operon of Lactobacillus sakei LTH681. System Appl Microbiol 22:321–328

    CAS  Google Scholar 

  • Segal G, Ron EZ (1996) Regulation and organization of the groE and dnaK operons in Eubacteria. FEMS Microbiol Lett 138:1–10

    Article  CAS  Google Scholar 

  • Serrano LM, Molenaar D, Wels M, Teusink B, Bron PA, de Vos WM, Smid EJ (2007) Thioredoxin reductase is a key factor in the oxidative stress response of Lactobacillus plantarum WCFS1. Microb Cell Fact 6:29

    Article  CAS  Google Scholar 

  • Serrazanetti D, Guerzoni ME, Corsetti A, Vogel R (2009) Metabolic impact and potential exploitation of the stress reactions in lactobacilli. Food Microbiol 26:700–711

    Article  CAS  Google Scholar 

  • Siegumfeldt H, Rechinger KB, Jakobsen M (2000) Dynamic changes of intracellular pH in individual lactic acid bacterium cells in response to a rapid drop in extracellular pH. Appl Environ Microbiol 66:2330–2335

    Article  CAS  Google Scholar 

  • Siragusa S, De Angelis M, Di Cagno R, Rizzello CG, Coda R, Gobbetti M (2007) Production of γ-aminobutyric acid (GABA) by lactic acid bacteria isolated from Italian cheese varieties. Appl Environ Microbiol 73(22):7283–7290

    Article  CAS  Google Scholar 

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

    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 

  • Stentz R, Loizel C, Mallert C, Zagorec M (2000) Development of genetic tools for Lactobacillus sakei: disruption of the β-galactosidase gene and Use of lacZ as a reporter gene to study regulation of the putative copper ATPase, AtkB. Appl Environ Microbiol 66:4272–4278

    Article  CAS  Google Scholar 

  • Stolz P, Böcker G, Hammes WP, Vogel RF (1995) Utilization of electron acceptors by lactobacilli isolated from sourdough. II. Lactobacillus pontis, L. reuteri, L. amylovorus, L. fermentum. Z Lebensm Unters Forsch 201:402–410

    Article  CAS  Google Scholar 

  • Streit F, Corrieu G, Béal C (2007) Acidification improves cryotolerance of Lactobacillus delbrueckii subsp. bulgaricus CFL1. J Biotechnol 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 

  • Stuart MR, Chou LS, Weimer BC (1999) Influence of carbohydrate starvation and arginine on culturability and amino acid utilization of Lactococcus lactis subsp. lactis. Appl Environ Microbiol 65:665–673

    CAS  Google Scholar 

  • Sturme MHJ, Kleerebezem M, Nakayama J, Akkermans ADL, Vaughan EE, de Vos WM (2002) Cell to cell communication by autoinducing peptides in Gram-positive bacteria. Antonie van Leeuwenhoek 81:233–243

    Article  CAS  Google Scholar 

  • Sturme MH, Nakayama J, Molenaar D, Murakami Y, Kunugi R, Fujii T, Vaughan EE, Kleerebezem M, de Vos WM (2005) An agr-like twocomponent regulatory system in Lactobacillus plantarum is involved in production of a novel cyclic peptide and regulation of adherence. J Bacteriol 187:5224–5235

    Article  CAS  Google Scholar 

  • Sturme MH, Francke JC, Siezen RJ, de Vos WM, Kleerebezem M (2007) Making sense of quorum sensing in lactobacilli: a special focus on Lactobacillus plantarum WCFS1. Microbiology 153:3939–3947

    Article  CAS  Google Scholar 

  • Sukharev SI, Blount P, Martinac B, Kung C (1997) Mechanosensitive channels of Escherichia coli: the MscL gene, protein, and activities. Annu Rev Physiol 59:633–657

    Article  CAS  Google Scholar 

  • Suokko A, Poutanen M, Savijoki K, Kalkkinen N, Varmanen P (2008) ClpL is essential for induction of thermotolerance and is potentially part of the HrcA regulon in Lactobacillus gasseri. Proteomics 8:1029–1041

    Article  CAS  Google Scholar 

  • Tieking M, Gaenzle MG (2005) Exopolysaccharides from cereal-associated lactobacilli. Trends Food Sci Technol 16:79–84

    Article  CAS  Google Scholar 

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

    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 

  • van de Guchte M, Penaud S, Grimaldi C, Barbe V, Bryson K, Nicolas P, Robert C, Oztas S, Mangenot S, Couloux A, LouxV, Dervyn R, Bossy R, Bolotin A, Batto JM, Walunas T, Gibrat JF, Bessieres P, Weissenbach J, Ehrlich SD, Maguin E (2006) The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proc Natl Acad Sci USA 103:9274–9279

    Article  CAS  Google Scholar 

  • Vermeulen N, Czerny M, Gänzle MG, Schieberle P, Vogel RF (2007) Reduction of (E)-2-nonenal and (E,E)-2,4-decadienal during sourdough fermentation. J Cereal Sci 45:78–87

    Article  CAS  Google Scholar 

  • Vernocchi P, Ndagijimana M, Serrazanetti D, Gianotti A, Vallicelli M, Guerzoni ME (2008) Influence of starch addition and dough microstructure on fermentation aroma production by yeasts and lactobacilli. Food Chem 108:1217–1225

    Article  CAS  Google Scholar 

  • Vogel RF, Pavlovic M, Hörmann S, Ehrmann MA (2005) High pressure-sensitive gene expression in Lactobacillus sanfranciscensis. Braz J Med Biol Res 38:1247–1252

    Article  CAS  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 

  • Warriner KRS, Morris JG (1995) The effects of aeration on the bioreductive abilities of some heterofermentative lactic acid bacteria. Lett Appl Microbiol 20:323–327

    Article  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zink R, Walker C, Schmidt G, Elli M, Pridmore D, Reniero R (2000) Impact of multiple stress factors on the survival of dairy lactobacilli. Sci Alim 20:119–126

    Article  CAS  Google Scholar 

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

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biologia e Chimica Agro-Forestale ed Ambientale, University of Bari, Via G. Amendola 165/a, 70125, Bari, Italy

    Maria De Angelis & Marco Gobbetti

Authors
  1. Maria De Angelis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marco Gobbetti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marco Gobbetti .

Editor information

Editors and Affiliations

  1. Laboratory of Dairy Research, Department of Food Science and Technolog, Agricultural University of Athens, Iera Odos 75, Athens, 118 55, Greece

    Effie Tsakalidou

  2. Laboratory of Dairy Research, Department of Food Science and Technolog, Agricultural University of Athens, Iera Odos 75, Athens, 188 55, Greece

    Konstantinos Papadimitriou

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

De Angelis, M., Gobbetti, M. (2011). Stress Responses of Lactobacilli. 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_11

Download citation

Publish with us

Policies and ethics

Search

Navigation