Skip to main content
SpringerLink
Log in
Book cover

Stress Responses of Lactic Acid Bacteria pp 67–90Cite as

Responses of Lactic Acid Bacteria to Osmotic Stress

  • Chapter
  • First Online:

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

Abstract

In industrial processes, during human infection, and in nature, lactic acid bacteria (LAB) are frequently exposed to adverse environmental conditions. Among the challenges posed by an ever-changing environment, osmotic stress is a prominent constraint that can stop cell growth and activate specific mechanisms that prevent cell death. This chapter will discuss the current knowledge about the molecular players that allow LAB to contend with hyper- and hypoosmotic stresses. We summarize how these bacteria control turgor by actively modulating the pool of osmotically active solutes in their cytoplasm. The major adaptive strategy to high osmolality is the intracellular accumulation of organic compounds, which are both effective osmoprotectants (efficient at increasing cytoplasmic osmolality, and growth rate) and compatible solutes (without deleterious effects on biopolymer functions, including stability and activity). Coupled with the movement and accumulation of solutes are the induction of stress proteins and the transcriptional regulation of key enzymes. In addition, the emerging mechanisms that sense and transduce the osmotic signal in the cell will be discussed.

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

  • Abranches J, Lemos JA, Burne RA (2006) Osmotic responses of Streptococcus mutans UA159. FEMS Microbiol Lett 255:240–246

    Article  CAS  Google Scholar 

  • Baliarda A, Robert H, Jebbar M, Blanco C, Deschamps A, Le Marrec C (2003a) Potential osmoprotectants for the lactic acid bacteria Pediococcus pentosaceus and Tetragenococcus halophila. Int J Food Microbiol 84:13–20

    Article  CAS  Google Scholar 

  • Baliarda A, Robert H, Jebbar M, Blanco C, Le Marrec C (2003b) Isolation and characterization of ButA, a secondary glycine betaine transport system operating in Tetragenococcus halophila. Curr Microbiol 47:347–351

    Article  CAS  Google Scholar 

  • Biemans-Oldehinkel E, Poolman B (2003) On the role of the two extracytoplasmic substrate-binding domains in the ABC transporter OpuA. EMBO J 22:5983–5993

    Article  CAS  Google Scholar 

  • Biemans-Oldehinkel E, Mahmood NA, Poolman B (2006) A sensor for intracellular ionic strength. Proc Natl Acad Sci USA 103:10624–10629

    Article  CAS  Google Scholar 

  • Bourdineaud JP, Nehmé B, Tesse S, Lonvaud-Funel A (2003) The ftsH gene of the wine bacterium Oenococcus oeni is involved in protection against environmental stress. Appl Environ Microbiol 69:2512–2520

    Article  CAS  Google Scholar 

  • Bourdineaud JP, Nehmé B, Tesse S, Lonvaud-Funel A (2004) A bacterial gene homologous to ABC transporters protects Oenococcus oeni from ethanol and other stress factors in wine. Int J Food Microbiol 92:1–14

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Caldas T, Demont-Caulet N, Ghazi A, Richarme G (1999) Thermoprotection by glycine betaine and choline. Microbiology 145:2543–2548

    CAS  Google Scholar 

  • Cayley S, Record MT (2004) Large changes in cytoplasmic biopolymer concentration with osmolality indicate that macromolecular crowding may regulate protein-DNA interactions and growth rate in osmotically stressed Escherichia coli K-12. J Mol Recog 17:488–496

    Article  CAS  Google Scholar 

  • Csonka LN, Epstein W (1996) Osmoregulation. In: Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (Eds.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, DC, pp.1210–1223

    Google Scholar 

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

    Article  Google Scholar 

  • Diamant S, Elaihu N, Rosenthal D, Goloubinoff P (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586–39591

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fang F, Flynn S, Li Y, Claesson MJ, van Pijkeren JP, Collins JK, van Sinderen D, O’Toole PW (2008) Characterization of endogenous plasmids from Lactobacillus salivarius UCC118. Appl Environ Microbiol 74:3216–3228

    Article  CAS  Google Scholar 

  • Flahaut S, Benachour A, Giard JC, Boutibonnes P, Auffray Y (1996) Defence against lethal treatments and de novo protein synthesis induced by NaCl in Enterococcus faecalis ATCC19433. Arch Microbiol 165:317–324

    Article  CAS  Google Scholar 

  • Flynn S (2001) Molecular characterisation of bacteriocin producing genes and plasmid encoded functions of the probiotic strain Lactobacillus salivarius subsp. salivarius UCC118. PhD thesis. University College Cork, Ireland

    Google Scholar 

  • Folgering JH, Moe PC, Schuurman-Wolters GK, Blount P, Poolman B (2005) Lactococcus lactis uses MscL as its principal mechanosensitive channel. J Biol Chem 280:8784–8792

    Article  CAS  Google Scholar 

  • Froger A, Rolland JP, Bron P, Lagrée V, Le Cahérec F, Deschamps S, Hubert JF, Pellerin I, Thomas D, Delamarche C (2001) Functional characterization of a microbial aquaglyceroporin. Microbiology 147:1129–1135

    CAS  Google Scholar 

  • Fukuda D, Watanabe M, Sonezaki S, Sugimoto S, Sonomoto K, Ishizaki A (2002) Molecular characterization and regulatory analysis of dnaK operon of halophilic lactic acid bacterium Tetragenococcus halophila. J Biosci Bioeng 93:388–394

    CAS  Google Scholar 

  • Giard JC, Rincé 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Glaasker E, Heuberger EH, Konings WN, Poolman B (1998b) Mechanism of osmotic activation of the quaternary ammonium compound transporter (QacT) of Lactobacillus plantarum. J Bacteriol 180:5540–5546

    CAS  Google Scholar 

  • Guillot A, Obis D, Mistou MY (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

    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  Google Scholar 

  • Hutkins RW, Ellefson WL, Kashket ER (1987) Betaine transport imparts osmotolerance on a strain of Lactobacillus acidophilus. Appl Environ Microbiol 53:2275–2281

    CAS  Google Scholar 

  • Ingraham JL, Marr AG (1996) Effects of temperature, pressure, pH, and osmotic stress on growth. In: Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (Eds.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, DC, pp. 1570–1578

    Google Scholar 

  • Itoi S, Abe T, Washio S, Ikuno E, Kanomata Y, Sugita H (2008) Isolation of halotolerant Lactococcus lactis subsp. lactis from intestinal tract of coastal fish. Int J Food Microbiol 21:116–121

    Article  Google Scholar 

  • Jewell JB, Kashket ER (1991) Osmotically regulated transport of proline by Lactobacillus acidophilus IFO 3532. Appl Environ Microbiol 57:2829–2833

    CAS  Google Scholar 

  • Jung H (2002) The sodium/substrate symporter family: structural and functional features. FEBS Lett 529:73–77

    Article  CAS  Google Scholar 

  • Kets EP, de Bont JAM (1994) Protective effects of betaine on survival of Lactobacillus plantarum subjected to drying. FEMS Microbiol Lett 116:251–256

    Article  CAS  Google Scholar 

  • Kets EP, Galinski EA, de Bont JAM (1994) Carnitine: a novel compatible solute in Lactobacillus plantarum. Arch Microbiol 162:243–248

    Article  CAS  Google Scholar 

  • Kets EP, Teunissen P, de Bont JAM (1996) Effect of compatible solutes on survival of lactic acid bacteria subjected to drying. Appl Environ Microbiol 62:259–261

    CAS  Google Scholar 

  • Kets EP, Groot M, Galinski EA, de Bont JAM (1997) Choline and acetylcholine: novel cationic osmolytes in Lactobacillus plantarum. Appl Microbiol Biotechnol 48:94–98

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Koch S, Oberson G, Eugster-Meier E, Meile L, Lacroix C (2007) Osmotic stress induced by salt increases cell yield, autolytic activity, and survival of lyophilization of Lactobacillus delbrueckii subsp. lactis. Int J Food Microbiol 117:36–42

    Article  CAS  Google Scholar 

  • Kurz M (2008) Compatible solute influence on nucleic acids: many questions but few answers. Saline Systems 4:6

    Google Scholar 

  • Le Breton Y, Pichereau V, Flahaut S, Auffray Y, Rincé A (2002) Identification of new genes related to osmotic adaptation in Enterococcus faecalis. Sci Alim 22:87–96

    Article  Google Scholar 

  • Le Marrec C, Bon E, Lonvaud-Funel A (2007) Tolerance to high osmolality of the lactic acid bacterium Oenococcus oeni and identification of potential osmoprotectants. Int J Food Microbiol 115:335–342

    Article  Google Scholar 

  • Liu Y, Bolen DW (1995) The peptide backbone plays a dominant role in protein stabilization by naturally occurring osmolytes. Biochemistry 34:12884–12891

    Article  CAS  Google Scholar 

  • Liu M, Hanks TS, Zhang J, McClure MJ, Siemsen DW, Elser J, Quinn MT, Lei B (2006) Defects in ex vivo and in vivo growth and sensitivity to osmotic stress of group A Streptococcus caused by interruption of response regulator vicR. Microbiol 152:967–978

    Article  CAS  Google Scholar 

  • Lorca GL, Barabote RD, Zlotopolski V, Tran C, Winnen B, Hvorup RN, Stonestrom AJ, Nguyen E, Huang LW, Kim DS, Saier MH Jr (2007) Transport capabilities of eleven Gram-positive bacteria: comparative genomic analyses. Biochim Biophys Acta 1768:1342–1366

    Article  CAS  Google Scholar 

  • Machado MC, Lopez CS, Heras H, Rivas EA (2004) Osmotic response in Lactobacillus casei ATCC 393: biochemical and biophysical characteristics of membrane. Arch Biochem Biophys 422:61–70

    Article  CAS  Google Scholar 

  • Mahmood NA, Biemans-Oldehinkel E, Poolman B (2009) Engineering of ion sensing by the cystathionine beta-synthase module of the ABC transporter OpuA. J Biol Chem 284:14368–14376

    Article  CAS  Google Scholar 

  • Marceau A, Zagorec M, Chaillou S, Méra T, Champomier-Vergès MC (2004) Evidence for involvement of at least six proteins in adaptation of Lactobacillus sakei to cold temperature and addition of NaCl. Appl Environ Microbiol 70:7260–7268

    Article  CAS  Google Scholar 

  • Mille Y, Obert JP, Beney L, Gervais P (2004) New drying process for lactic bacteria based on their dehydration behavior in liquid medium. Biotechnol Bioeng 88:71–76

    Article  CAS  Google Scholar 

  • Mille Y, Beney L, Gervais P (2005) Compared tolerance to osmotic stress in various microorganisms: towards a survival prediction test. Biotechnol Bioeng 92:479–484

    Article  CAS  Google Scholar 

  • Molenaar D, Hagting A, Alkema H, Driessen AJ, Konings WN (1993) Characteristics and osmoregulatory roles of uptake systems for proline and glycine betaine in Lactococcus lactis. J Bacteriol 175:5438–5444

    CAS  Google Scholar 

  • Molina-Höppner A, Doster W, Vogel RF, Gänzle MG (2004) Protective effect of sucrose and sodium chloride for Lactococcus lactis during sublethal and lethal high-pressure treatments. Appl Environ Microbiol 70:2013–2020

    Article  Google Scholar 

  • Obis D, Guillot A, Gripon JC, Renault P, Bolotin A, Mistou MY (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

    CAS  Google Scholar 

  • Obis D, Guillot A, Mistou MY (2001) Tolerance to high osmolality of Lactococcus lactis subsp. lactis and cremoris is related to the activity of a betaine transport system. FEMS Microbiol Lett 202:39–44

    Article  CAS  Google Scholar 

  • O’Connell-Motherway M, van Sinderen D, Morel-Deville F, Fitzgerald GF, Ehrlich SD, Morel P (2000) Six putative two-component regulatory systems isolated from Lactococcus lactis subsp. cremoris MG1363. Microbiology 146:935–947

    Google Scholar 

  • Patzlaff JS, van der Heide T, Poolman B (2003) The ATP/substrate stoichiometry of the ATP-binding cassette (ABC) transporter OpuA. J Biol Chem 278:29546–29551

    Article  CAS  Google Scholar 

  • Pichereau V, Bourot S, Flahaut S, Blanco C, Auffray Y, Bernard T (1999) The osmoprotectant glycine betaine inhibits salt-induced cross-tolerance towards lethal treatment in Enterococcus faecalis. Microbiology 145:427–435

    Article  CAS  Google Scholar 

  • Piuri M, Sanchez-Rivas C, Ruzal SM (2003) Adaptation to high salt in Lactobacillus: role of peptides and proteolytic enzymes. J Appl Microbiol 95:372–379

    Article  CAS  Google Scholar 

  • Piuri M, Sanchez-Rivas C, Ruzal SM (2005) Cell wall modifications during osmotic stress in Lactobacillus casei. J Appl Microbiol 98:84–95

    Article  CAS  Google Scholar 

  • Poirier I, Marechal PJ, Gervais P (1997) Effects of kinetics of water potential variation on bacterial viability. J Appl Microbiol 82:101–106

    Article  CAS  Google Scholar 

  • Poirier I, Marechal PJ, Gervais P (1998) Escherichia coli and Lactobacillus plantarum responses to osmotic stress. Appl Microbiol Biotechnol 50:704–709

    Article  CAS  Google Scholar 

  • Prasad J, McJarrow P, Gopal P (2003) Heat and osmotic stress responses of probiotic Lactobacillus rhamnosus HN001 (DR20) in relation to viability after drying. Appl Environ Microbiol 69:917–925

    Article  CAS  Google Scholar 

  • Robert H, Le Marrec C, Blanco C, Jebbar M (2000) Glycine betaine, carnitine, and choline enhance salinity tolerance and prevent the accumulation of sodium to a level inhibiting growth of Tetragenococcus halophila. Appl Environ Microbiol 66:509–517

    Article  CAS  Google Scholar 

  • Romantsov T, Guan Z, Wood JM (2009) Cardiolipin and the osmotic stress responses of bacteria. Biochim Biophys Acta 1788:2092–2100

    Article  CAS  Google Scholar 

  • Romeo Y, Obis D, Bouvier J, Guillot A, Fourçans A, Bouvier I, Gutierrez C, Mistou MY (2003) Osmoregulation in Lactococcus lactis: BusR, a transcriptional repressor of the glycine betaine uptake system BusA. Mol Microbiol 47:1135–1147

    Article  CAS  Google Scholar 

  • Romeo Y, Bouvier J, Gutierrez C (2007) Osmotic regulation of transcription in Lactococcus lactis: ionic strength-dependent binding of the BusR repressor to the busA promoter. FEBS Lett 581:3387–3390

    Article  CAS  Google Scholar 

  • Santivarangkna C, Kulozik U, Foerst P (2008a) Inactivation mechanisms of lactic acid starter cultures preserved by drying processes. J Appl Microbiol 105:1–13

    Article  CAS  Google Scholar 

  • Santivarangkna C, Higl B, Foerst P (2008b) Protection mechanism of sugars during stages of preparation process during dried lactic acid starter cultures. Food Microbiol 25:429–441

    Article  CAS  Google Scholar 

  • Shabala L, Bowman J, Brown J, Ross T, McMeekin T, Shaabala S (2009) Ion transport and osmotic adjustment in response to ionic and non-ionic osmotic. Environ Microbiol 11:137–148

    Article  CAS  Google Scholar 

  • Sheehan VM, Sleator RD, Fitzgerald GF, Hill C (2006) Heterologous expression of BetL, a betaine uptake system, enhances the stress tolerance of Lactobacillus salivarius UCC118. Appl Environ Microbiol 72:2170–2177

    Article  CAS  Google Scholar 

  • Sheehan VM, Sleator RD, Hill C, Fitzgerald GF (2007) Improving gastric transit, gastrointestinal persistence and therapeutic efficacy of the probiotic strain Bifidobacterium breve UCC2003. Microbiology 153:3563–3571

    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 

  • Smith LT (1996) Role of osmolytes in adaptation of osmotically stressed and chill-stressed Listeria monocytogenes grown in liquid media and on processed meat surfaces. Appl Environ Microbiol 62:3088–3093

    CAS  Google Scholar 

  • Sunny-Roberts EO, Knorr D (2008) Evaluation of the response of Lactobacillus rhamnosus VTT E-97800 to sucrose-induced osmotic stress. Food Microbiol 25:183–189

    Article  CAS  Google Scholar 

  • Svensäter G, Sjögreen B, Hamilton IR (2000) Multiple stress responses in Streptococcus mutans and the induction of general and stress-specific proteins. Microbiology 146:107–117

    Google Scholar 

  • Tymczyszyn EE, Gómez-Zavaglia A, Disalvo EA (2005) Influence of the growth at high ­osmolality on the lipid composition, water permeability and osmotic response of Lactobacillus bulgaricus. Arch Biochem Biophys 443:66–73

    Article  CAS  Google Scholar 

  • Uguen P, Hamelin, J, Le Pennec JP, 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

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • van der Heide T, Poolman B (2000b) Osmoregulated ABC-transport system of Lactococcus lactis senses water stress via changes in the physical state of the membrane. Proc Natl Acad Sci USA 97:7102–7106

    Article  Google Scholar 

  • Velamakanni S, Lau CH, Gutmann DA, Venter H, Barrera NP, Seeger MA, Woebking B, Matak-Vinkovic D, Balakrishnan L, Yao Y, U EC, Shilling RA, Robinson CV, Thorn P, van Veen HW (2009) A multidrug ABC transporter with a taste for salt. PLoS One 4:6137

    Article  Google Scholar 

  • Welsh DT (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 24:263–290

    Article  CAS  Google Scholar 

  • Whatmore AM, Reed RH (1990) Determination of turgor pressure in Bacillus subtilis: possible role for K  +  in turgor regulation. J Gen Microbiol 136:2521–2526

    CAS  Google Scholar 

  • Xie Y, Chou LS, Cutler A, Weimer B (2004) DNA macroarray profiling of Lactococcus lactis subsp. lactis IL1403 gene expression during environmental stresses. Appl Environ Microbiol 70:6738–6747

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Dr. Marguerite Dols and Prof. Mohamed Jebbar are gratefully acknowledged for their helpful comments as well as Cate Evans for her help in preparing the manuscript.

Author information

Authors and Affiliations

  1. Ecole Nationale Supérieure de Chimie Biologie Physique, Institut Polytechnique de Bordeaux, Unité de Recherche Œnologie - EA 4577 - USC 1219 INRA., Institut des Sciences de la Vigne et du Vin, 210 Chemin de Leysotte, CS50008, Villenave d’Ornon, France

    Claire Le Marrec

Authors
  1. Claire Le Marrec
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claire Le Marrec .

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

Le Marrec, C. (2011). Responses of Lactic Acid Bacteria to Osmotic 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_4

Download citation

Publish with us

Policies and ethics

Search

Navigation