Stress Responses of Oenococcus oeni

  • Jean Guzzo
Part of the Food Microbiology and Food Safety book series (FMFS)


Oenococcus oeni is an alcohol-tolerant, acidophilic lactic acid bacterium responsible for malolactic fermention in wine. The stress responses of O. oeni have been studied at both the molecular and physiological levels. Genes encoding stress proteins mainly belong to the CtsR regulon. Other regulation mechanisms seem to coexist in O. oeni and may correspond to posttranscriptional regulation. Maintenance of the cell membrane integrity under stress conditions seems to be a prerequisite for survival in wine. The active cell response to protect membrane function under stress conditions requires changes in fatty acid composition and involves stress proteins. Various solute transporters and energy transduction systems contribute to the survival of O. oeni cells by regulating the change of internal and external pH. Finally, knowledge of the genome sequence of two O. oeni strains provides essential data, which will be discussed in this chapter.


Lactic Acid Bacterium Acid Tolerance Cyclopropane Fatty Acid Membrane Fatty Acid Composition Oeni Strain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Alexandre H, Costello PJ, Remize F, Guzzo J, Guilloux-Benatier M (2004) Saccharomyces cerevisiae-Oenococcus oeni interactions in wine: current knowledge and perspectives. Int J Food Microbiol 93:141–154CrossRefGoogle Scholar
  2. Assad-Garcia, JS, Guzzo J, Grandvalet C (2008) An improved protocol for electroporation of oenococcus oeni ATCC BAA-1163 using ethanol as immediate membrane fluidizing agent. Lett Appl Microbiol 47:333–338CrossRefGoogle Scholar
  3. Augagneur Y, Ritt JF, Linares DM, Remize F, Tourdot-Maréchal R, Garmyn D, Guzzo J (2007) Dual effect of organic acids as a function of external pH in Oenococcus oeni. Arch Microbiol 188:147–157CrossRefGoogle Scholar
  4. Bartowsky EJ (2005) Oenococcus oeni and malolactic fermentation – moving into the molecular arena. Austral J Grape Wine Res 11:174–187CrossRefGoogle Scholar
  5. Beltramo C, Oraby M, Bourel G, Garmyn D, Guzzo J (2004a) A new vector, pGID052, for genetic transfer in Oenococcus oeni. FEMS Microbiol Lett 236:53–60Google Scholar
  6. Beltramo C, Grandvalet C, Guzzo J (2004b) Evidence for multiple levels of regulation of Oenococcus oeni clpP-clpL locus expression in response to stress. J Bacteriol 186:2200–2205CrossRefGoogle Scholar
  7. Beltramo C, Desroche N, Tourdot-Maréchal R, Grandvalet C, Guzzo J (2006) Real-time PCR for characterizing the stress response of Oenococcus oeni in a wine-like medium. Res Microbiol 157:267–274CrossRefGoogle Scholar
  8. Bon E, Delaherche A, Bilhère E, De Daruvar, A, Lonvaud-Funel A, Le Marrec C (2009) Oenococcus oeni genome plasticity is associated with fitness. Appl Environ Microbiol 75:2079–2090CrossRefGoogle Scholar
  9. 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 69:2512–2520CrossRefGoogle Scholar
  10. Bourdineaud JP, Nehmé B, Tesse S, Lonvaud-Funel A (2004) A bacterial gene homologous to ABC transporters protect Oenococcus oeni ethanol and other stress factors in wine. Int J Food Microbiol 92:1–14CrossRefGoogle Scholar
  11. Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125:443–451CrossRefGoogle Scholar
  12. Carreté R, Vidal MT, Bordons A, Constanti M (2002) Inhibitory effect of sulfur dioxide and other stress compounds in wine on the ATPase activity of Oenococcus oeni. FEMS Microbiol Lett 211:155–159CrossRefGoogle Scholar
  13. Cavin JF, Prevost H, Lin J, Schmitt P, Divies C (1989) Medium for screening Leuconostoc oenos strains defective in malolactic fermentation. Appl Environ Microbiol 62:1274–1282Google Scholar
  14. 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 1717:118–124CrossRefGoogle Scholar
  15. Coucheney F, Desroche N, Bou M, Tourdot-Maréchal R, Dulau L, Guzzo J (2005a) A new approach for selection of Oenococcus oeni strains in order to produce malolactic starter. Int J Food Microbiol 105:463–470CrossRefGoogle Scholar
  16. Coucheney F, Gal L, Beney L, Lherminier J, Gervais P, Guzzo J (2005b) A small HSP, Lo18 interacts with the cell membrane and modulates lipid physical state under heat shock conditions in a lactic acid bacterium. Biochim Biophys Acta 1720:92–98CrossRefGoogle Scholar
  17. Da Silveira MG, Abee T (2009) Activity of ethanol-stressed Oenococcus oeni cells: a flow cytometric approach. J Appl Microbiol 106:1690–1696CrossRefGoogle Scholar
  18. Da Silveira MG, Golovina EA, Hoekstra FA, Rombouts FM, Abee T (2003) Membrane fluidity adjustments in ethanol-stressed Oenococcus oeni cells. Appl Environ Microbiol 69:5826–5832CrossRefGoogle Scholar
  19. Da Silveira MG, Buamgärtner M, Rombouts FM, Abee T (2004) Effect of adaptation to ethanol on cytoplasmic and membrane protein profiles of Oenococcus oeni. Appl Env Microbiol 70: 2748–2755CrossRefGoogle Scholar
  20. De las Rivas B, Marcobal A, Munoz R (2004) Allelic diversity and population structure in Oenococcus oeni as determined from sequence analysis of housekeeping genes. Appl Environ Microbiol 70:7210–7219Google Scholar
  21. Delmas F, Diviès C, Guzzo J (2001) In vitro and in vivo studies of the membrane associated small heat shock protein Lo18 from the lactic acid bacterium Oenococcus oeni. J Mol Microbiol Biotechnol 3:601–610Google Scholar
  22. 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 31:117–131CrossRefGoogle Scholar
  23. Dicks LM, Dellaglio F, Collins MD (1995) Proposal to reclassify Leuconostoc oenos as Oenococcus oeni. Int J Syst Bacteriol 45:395–397CrossRefGoogle Scholar
  24. Dols-Lafargue M, Lee HY, Le Marrec C, Heyraud A, Chambat G, Lonvaud-Funel A (2008) Characterization of gtf, a glucosyltransferase gene in the genome of Pediococcus parvulus and Oenococcus oeni, two bacterial species commonly found in wine. Appl Environ Microbiol 74:4079–4090CrossRefGoogle Scholar
  25. Drici-Cachon Z, Cavin JF, Divies C (1996) Effect of pH and age of culture on cellular fatty acid composition of Leuconostoc oenos. Lett Appl Microbiol 22:331–334CrossRefGoogle Scholar
  26. Figueiredo AR, Campos F, de Freitas V, Hogg T, Couto JA (2008) Effect of phenolic aldehydes and flavonoids on growth and inactivation of Oenococcus oeni and Lactobacillus hilgardii. Food Microbiol 25:105–112CrossRefGoogle Scholar
  27. Fortier LC, Tourdot-Maréchal R, Lee BH, Diviès C, Guzzo J (2003) Induction of Oenococcus oeni H+-ATPase activity and mRNA transcription under acidic conditions of growth. FEMS Microbiol Lett 222:165–169CrossRefGoogle Scholar
  28. Galland D, Tourdot-Maréchal R, Abraham M, Chu Ky S, Guzzo J (2003) Absence of malolactic activity is a characteristic of H+-ATPase deficient mutants from the lactic acid bacterium Oenococcus oeni. Appl Environ Microbiol 69:1973–1979CrossRefGoogle Scholar
  29. Garbay S, Lonvaud-Funel A (1996) Response of Leuconostoc oenos to environmental changes. J Appl Bacteriol 81:619–625Google Scholar
  30. Garbay S, Rozès N, Lonvaud-Funel A (1995) Fatty acid composition of Leuconostoc oenos, incidence of growth conditions and relationship with malolactic efficiency. Food Microbiol 12:387–395CrossRefGoogle Scholar
  31. Giese KC, Vierling E (2004) Mutants in a small heat shock protein that affect the oligomeric state. J Biol Chem 279:32674–32683CrossRefGoogle Scholar
  32. Grandvalet C, Coucheney F, Beltramo F, Guzzo J (2005) CtsR is the master regulator of stress response gene expression in Oenococcus oeni. J Bacteriol 187:5614–5623CrossRefGoogle Scholar
  33. Grandvalet C, Assad-Garcia JS, Chu Ky S, Tollot M, Guzzo J, Gresti J, Tourdot-Maréchal R (2008) Changes in membrane lipid composition in ethanol and acid adapted Oenococcus oeni cells: characterization of the CFA gene by heterologous recombination. Microbiology 154:2611–2619CrossRefGoogle Scholar
  34. Guilloux-Bénatier M, Remize F, Gal L, Guzzo J, Alexandre H (2006) Effects of yeast proteolytic activity on Oenococcus oeni and malolactic fermentation. FEMS Microbiol Lett 263:183–188CrossRefGoogle Scholar
  35. Guzzo J, Desroche N (2009) Physical and chemical stress factors in lactic acid bacteria. In: König H, Unden G, Fröhlich J (Eds.), Biology of microorganisms on grapes, in must and in wine. Springer-Verlag, Berlin, pp. 295–308Google Scholar
  36. Guzzo J, Cavin JF, Divies C (1994) Induction of stress proteins in Leuconostoc oenos to perform direct inoculation of wine. Biotechnol Lett 16:1189–1194CrossRefGoogle Scholar
  37. Guzzo J, Delmas F, Pierre F, Jobin MP, Samyn B, Van Beeumen J, Cavin JF, Diviès C (1997) A small heat shock protein from Leuconostoc oenos induced by multiple stresses and during stationary growth phase. Lett Appl Microbiol 24:393–396CrossRefGoogle Scholar
  38. Guzzo J, Jobin MP, Diviès C (1998) Increase of sulfite tolerance in Oenococcus oeni by means of acidic adaptation. FEMS Microbiol Lett 160:43–47CrossRefGoogle Scholar
  39. Ibarburu I, Soria-Diaz ME, Rodriguez-Carvajal MA, Velasco SE, Tejero-Mateo P, Gil-Serrano AM, Irastorza A, Duenas MT (2007) Growth and exopolysaccharide (EPS) production by Oenococcus oeni I4 and structural characterization of their EPSs. J Appl Microbiol 103:477–486CrossRefGoogle Scholar
  40. Jobin MP, Delmas F, Garmyn D, Diviès C, Guzzo J (1997) Molecular characterization of the gene encoding a 18-kDa small heat shock protein associated with the membrane of Leuconostos oenos. Appl Env Microbiol 63:609–614Google Scholar
  41. Jobin MP, Garmyn D, Diviès C, Guzzo J (1999a) Expression of the Oenococcus oeni trxA gene is induced by hydrogen peroxide and heat shock. Microbiology 145:1245–1251CrossRefGoogle Scholar
  42. Jobin MP, Garmyn D, Diviès C, Guzzo J (1999b) The Oenococcus oeni clpX homologue is a heat shock gene preferentially expressed in exponential growth phase. J Bacteriol 181:6634–6641Google Scholar
  43. Kirstein J, Dougan DA, Gerth U, Kecker M, Turgay K (2007) The tyrosine kinase McsB is a regulated adaptor protein for ClpCP. EMBO J 26:2061–2070CrossRefGoogle Scholar
  44. Kobayashi H, Suzuki T, Unemoto T (1986) Streptococcal cytoplasmic pH is regulated by changes in amount and activity of a proton-translocating ATPase. J Biol Chem 261:627–630Google Scholar
  45. Kunkee RE (1991) Some roles of malic acid in the malolactic fermentation in wine making. FEMS Microbiol Lett 88:55–71Google Scholar
  46. Labarre C, Guzzo J, Cavin JF, Diviès C (1996) Cloning and characterization of the genes encoding the malolactic enzyme and the malate permease of Leuconostoc oenos. Appl Environ Microbiol 62:1274–1282Google Scholar
  47. Lee GJ, Vierling E (2000) A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denaturated protein. Plant Physiol 122:189–198CrossRefGoogle Scholar
  48. Marcobal AM, Sela DA, Wolf YI, Makarova KS, Mills DA (2008) Role of hypermutability in the evolution of the genus Oenococcus. J Bacteriol 190:564–570CrossRefGoogle Scholar
  49. Matic I, Rayssiguier C, Radman M (1995) Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species. Cell 80:507–515CrossRefGoogle Scholar
  50. Mills DA, Rawsthorne H, Parker C, Tamir D, Makarova K (2005) Genomic analysis of Oenococcus oeni PSU-1 and its relevance to winemaking. FEMS Microbiol Lett 29:465–475Google Scholar
  51. Nakamoto H, Vigh L (2007) The small heat shock proteins and their clients. Cell Mol Life Sci 64:294–306CrossRefGoogle Scholar
  52. Olguin N, Bordons A, Reguant C (2009) Influence of ethanol and pH on the gene expression of the citrate pathway in Oenococcus oeni. Food Microbiol 26:197–203CrossRefGoogle Scholar
  53. Osborne JP, Edwards CG (2007) Inhibition of malolactic fermentation by a peptide produced by Saccharomyces cerevisiae during alcoholic fermentation. Int J Food Microbiol 118:27–34CrossRefGoogle Scholar
  54. Ramos A, Lolkema JS, Konings, WN, Santos H (1995) Enzyme basis for pH regulation of citrate and pyruvate metabolism by Leuconostoc oenos. Appl Environ Microbiol 61:1303–1310Google Scholar
  55. Remize F, Augagneur Y, Guilloux-Bénatier M, Guzzo J (2005) Effect of nitrogen limitation and nature of the feed upon Oenococcus oeni metabolism and extracellular protein production. J Appl Microbiol 98:652–661CrossRefGoogle Scholar
  56. Remize F, Gaudin A, Kong Y, Guzzo J, Alexandre H, Krieger S, Guilloux-Bénatier M (2006) Oenococcus oeni preference for peptides: qualitative and quantitative analysis of nitrogen assimilation. Arch Microbiol 185:459–469CrossRefGoogle Scholar
  57. Ritt JF, Guilloux-Benatier M, Guzzo J, Alexandre H, Remize F (2008) Oligopeptides assimilation and transport by Oenococcus oeni. J Appl Microbiol 104:573–580Google Scholar
  58. Salema M, Lolkema JS, San Romao MV, Loureiro Dias MC (1996) The proton motive force generated in Leuconostoc oenos by malate fermentation. J Bacteriol 178:3127–3132Google Scholar
  59. Teixeira H, Gonçalves MG, Rozès N, Ramos A, San Romao MV (2002) Lactobacillic acid accumulation in the plasma membrane of Oenococcus oeni: a response to ethanol stress. Microbiol Ecol 43:146–153CrossRefGoogle Scholar
  60. Tonon T, Bourdineaud JP, Lonvaud-Funel A (2001) The arcABC gene cluster encoding the arginine deiminase pathway of Oenococcus oeni, and arginine induction of a CRP-like gene. Res Microbiol 152:653–661CrossRefGoogle Scholar
  61. Török Z, Horvath I, Goloubinoff P, Kovacs E, Glatz A, Balogh G, Vigh L (1997) Evidence for a lipochaperonin: association of active protein-folding GroESL oligomers with lipids can stabilize membranes under heat shock conditions. Proc Natl Acad Sci USA 94:2192–2197CrossRefGoogle Scholar
  62. Török Z, Goloubinoff P, Horvath I, Tsvetkova NM, Glatz A, Balogh G, Varvasovszki V, Los DA, Vierling E, Crowe JH, Vigh L (2001) Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stresses membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc Natl Acad Sci USA 98:3098–3103CrossRefGoogle Scholar
  63. Tourdot-Maréchal R, Fortier LC, Guzzo J, Lee B, Diviès C (1999) Acid sensitivity of neomycin resistant mutants of Oenococcus oeni: a relationship between reduction of ATPase activity and lack of malolactic activity. FEMS Microbiol Lett 178:319–326CrossRefGoogle Scholar
  64. Watson K (1990) Microbial stress proteins. Adv Microbial Physiol 31:183–223CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Equipe de Recherche en Vigne et Vin, Institut Jules GuyotUniversité de BourgogneDijonFrance

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