Skip to main content
SpringerLink
Log in

Physical and Chemical Stress Factors in Lactic Acid Bacteria

  • Chapter
  • First Online:
Biology of Microorganisms on Grapes, in Must and in Wine

Abstract

The parameters influencing the malolactic fermentation (MLF) in wine are multiple. The winemaking process methods can be critical, but the main cause of delay appears to be the physical and chemical factors especially ethanol content, acidic pH, temperature, sulfites, or compounds present in the wine. Indeed, the cumulative effect of these multiple stresses increases the limitation for bacterial growth. However, several adaptative mechanisms at the genetical and physiological levels are implied for bacterial development and adaptation in wine. Some of them are discussed in this chapter.

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

Access this chapter

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 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
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

Similar content being viewed by others

References

  • Abee T, Wouters JA (1999) Microbial stress response in minimal processing. Int J Food Microbiol 50:65–91

    Article  CAS  PubMed  Google Scholar 

  • Alegria EG, Lopez I, Ruiz JI, Saenz J, Fernandez E, Zarazaga M, Dizy M, Torres C, Ruiz-Larrea F (2004) High tolerance of wild Lactobacillus plantarum and Oenococcus oeni strains to lyophilisation and stress environmental conditions of acid pH and ethanol. FEMS Microbiol Lett 230:53–61

    Article  CAS  Google Scholar 

  • 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 93:141–154

    Article  CAS  PubMed  Google Scholar 

  • Andorra I, Landi S, Mas A, Guillamon J, Esteve-Zarzoso B (2008) Effect of oenological practices on microbial populations using culture-independent techniques. Food Microbiol 25:849–856

    Article  CAS  PubMed  Google Scholar 

  • Augagneur Y, Ritt JF, Linares D, Remize F, Tourdot-Marechal R, Garmyn D, Guzzo J (2007) Dual effect of organic acids as a function of external pH in Oenococcus oeni. Arch Microbiol 188:147–157

    Article  CAS  PubMed  Google Scholar 

  • Bartowsky E (2009) Bacterial spoilage of wine and approaches to minimize it. Lett Appl Microbiol 48:149–156

    Article  CAS  PubMed  Google Scholar 

  • Bastard A, Coelho C, Briandet R, Canette A, Gougeon R, Alexandre H, Guzzo J, Weidmann S (2016) Effect of biofilm formation by Oenococcus oeni on malolactic fermentation and the release of aromatic compounds in wine. Front Microbiol 7:613

    Article  PubMed  PubMed Central  Google Scholar 

  • Belguendouz T, Cachon R, Divies C (1997) pH homeostasis and citric acid utilization: differences between Leuconostoc mesenteroides and Lactococcus lactis. Curr Microbiol 35:233–236

    Article  CAS  Google Scholar 

  • Beltramo C, Grandvalet C, Pierre F, Guzzo J (2004) Evidence for multiple levels of regulation of Oenococcus oeni clpP-clpL locus expression in response to stress. J Bacteriol 186:2200–2205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beltramo C, Desroche N, Tourdot-Marechal R, Grandvalet C, Guzzo J (2006) Real-time PCR for characterizing the stress response of Oenococcus oeni in a wine-like medium. Res Microbiol 157:267–274

    Article  CAS  PubMed  Google Scholar 

  • Betteridge A, Grbin P, Jiranek V (2015) Improving Oenococcus oeni to overcome challenges of wine malolactic fermentation. Trends Biotechnol 33:547–553

    Article  CAS  PubMed  Google Scholar 

  • Bonnin-Jusserand M, Grandvalet C, David V, Alexandre H (2011) Molecular cloning, heterologous expression, and characterization of Ornithine decarboxylase from Oenococcus oeni. J Food Prot 74:1309–1314

    Article  CAS  PubMed  Google Scholar 

  • Bordas M, Araque I, Alegret J, El Khoury M, Lucas P, Rozès N, Reguant C, Bordons A (2013) Isolation, selection, and characterization of highly ethanol-tolerant strains of Oenococcus oeni from south Catalonia. Int Microbiol 16:113–123

    CAS  PubMed  Google Scholar 

  • Borneman A, McCarthy J, Chambers P, Bartowsky E (2012) Comparative analysis of the Oenococcus oeni pan genome reveals genetic diversity in industrially-relevant pathway. BMC Genomics 13:373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bravo-Ferrada BM, Hollmann A, Delfederico L, Valdés La Hens D, Caballero A, Semorile L (2013) Patagonian red wines: selection of Lactobacillus plantarum isolates as potential starter cultures for malolactic fermentation. World J Microbiol Biotechnol 29:1537–1549

    Article  CAS  PubMed  Google Scholar 

  • Bravo-Ferrada M, Gómez-Zavaglia A, Semorile L, Tymczyszyn E (2014) Effect of the fatty acid composition of acclimated oenological Lactobacillus plantarum on the resistance to ethanol. Lett Appl Microbiol 60:155–161

    Article  PubMed  CAS  Google Scholar 

  • Britz TJ, Tracey RP (1990) The combination effect of pH, SO2, ethanol and temperature on the growth of Leuconostoc oenos. J Appl Bacteriol 68:23–31

    Article  CAS  Google Scholar 

  • Cabras P, Meloni M, Melis M, Farris GA, Budroni M, Satta T (1994) Interactions between lactic bacteria and fungicides during lactic fermentation. J Wine Res 5(1):53–59

    Article  Google Scholar 

  • Campbell-Sills H, El Khoury M, Favier M, Romano A, Biasioli F, Spano G, Sherman D, Bouchez O, Coton E, Coton M, Okada S, Tanaka N, Dols-Lafarge M, Lucas P (2015) Phylogenomic analysis of Oenococcus oeni reveals specific domestication of strains to cider and wines. Genome Biol Evol 7:1506–1518

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Campos FM, Couto JA, Hogg TA (2003) Influence of phenolic acids on growth and inactivation of Oenococcus oeni and Lactobacillus hilgardii. J Appl Microbiol 94:167–174

    Article  CAS  PubMed  Google Scholar 

  • Campos F, Figueiredo A, Hogg T, Couto J (2009a) Effect of phenolic acids on glucose and organic acid metabolism by lactic acid bacteria from wine. Food Microbiol 26:409–414

    Article  CAS  PubMed  Google Scholar 

  • Campos F, Couto JA, Figueiredo A, Toth IV, Rangel A, Hogg T (2009b) Cell damage induced by phenolic acids on wine lactic acid bacteria. Int J Food Microbiol 135:144–151

    Article  CAS  PubMed  Google Scholar 

  • Capozzi V, Weidmann S, Fiocco D, Rieu A, Hols P, Guzzo J, Spano G (2011) Inactivation of a small heat shock protein affects cell morphology and membrane fluidity in Lactobacillus plantarum WCFS1. Res Microbiol 162:419–425

    Article  CAS  PubMed  Google Scholar 

  • Capucho I, San Romao MV (1994) Effect of ethanol and fatty acids on malolactic activity of Leuconostoc oenos. Appl Microbiol Biotechnol 42:391–395

    CAS  Google Scholar 

  • Carrete 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 211:155–159

    Article  CAS  PubMed  Google Scholar 

  • Chang IS, Kim BH, Shin PK (1997) Use of sulfite and hydrogen peroxide to control bacterial contamination in ethanol fermentation. Appl Environ Microbiol 63:1–6

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chasseriaud L, Krieger-Weber S, Déléris-Bou M, Sieczkowski N, Jourdes M, Teissedre PL, Claisse O, Lonvaud-Funel A (2015) Hypotheses in the effects of oenological tannins and total red wine phenolic compounds on Oenococcus oeni. Food Microbiol 52:131–137

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Claisse O, Lonvaud-Funel A (2014) Multiplex variable number tandem repeats for Oenococcus oeni and applications. Food Microbiol 38:80–86

    Article  CAS  PubMed  Google Scholar 

  • Comitini F, Ferretti R, Clementi F, Mannazzu I, Ciani M (2005) Interactions between Saccharomyces cerevisiae and malolactic bacteria: preliminary characterization of a yeast proteinaceous compound(s) active against Oenococcus oeni. J Appl Microbiol 99:105–111

    Article  CAS  PubMed  Google Scholar 

  • Costantini A, Rantsiou K, Majumder A, Jacobsen S, Pessione E, Svenssorf B, Garcia-Moruno E, Cocolin L (2015) Complementing DIGE proteomics and DNA subarray analyses to shed light on Oenococcus oeni adaptation to ethanol in wine-simulated conditions. J Proteomics 123:114–127

    Article  CAS  PubMed  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 (table of contents)

    Google Scholar 

  • Coucheney F, Gal L, Beney L, Lherminier J, Gervais P, Guzzo J (2005a) 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 1720:92–98

    Article  CAS  PubMed  Google Scholar 

  • Coucheney F, Desroche N, Bou M, Tourdot-Maréchal R, Dulau L, Guzzo J (2005b) A new approach for selection of Oenococcus oeni strains in order to produce malolactic starters. Int J Food Microbiol 105:463–470

    Article  CAS  PubMed  Google Scholar 

  • Cronan J (2002) Phospholipid modifications in bacteria. Curr Opin Microbiol 5:202–205

    Article  CAS  PubMed  Google Scholar 

  • Da Silveira MG, San Romao VM, Loureiro-Dias MC, Rombouts FM, Abee T (2002) Flow cytometric assessment of membrane integrity of ethanol-stressed Oenococcus oeni cells. Appl Environ Microbiol 68:6087–6093

    Article  CAS  Google Scholar 

  • Da Silveira MG, Golovina EA, Hoekstra FA, Rombouts FM, Abee T (2003) Membrane fluidity adjustments in ethanol-stressed Oenococcus oeni cells. Appl Environ Microbiol 69:5826–5832

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Da Silveira MG, Baumgartner M, Rombouts FM, Abee T (2004) Effect of adaptation to ethanol on cytoplasmic and membrane protein profiles of Oenococcus oeni. Appl Environ Microbiol 70:2748–2755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis CR, Wibowo D, Eschenbruch R, Lee TH, Fleet GH (1985) Practical implications of malolactic fermentation: a review. Am J Enol Vitic 36:290–301

    CAS  Google Scholar 

  • Denich T, Beaudette L, Lee H, Trevors J (2003) Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J Microbiol Methods 52:149–182

    Article  CAS  PubMed  Google Scholar 

  • Drlica K (1992) Control of bacterial DNA supercoiling. Mol Microbiol 6:425–433

    Article  CAS  PubMed  Google Scholar 

  • du Toit M, Engelbrecht L, Lerm E, Krieger-Weber S (2011) Lactobacillus: the next generation of malolactic fermentation starter cultures—an overview. Food Bioproc Tech 4:876–906

    Article  Google Scholar 

  • Farias ME, Manca de Nadra MC (2000) Purification and partial characterization of Oenococcus oeni exoprotease. FEMS Microbiol Lett 185:263–266

    Article  CAS  PubMed  Google Scholar 

  • 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 25:105–112

    Article  CAS  PubMed  Google Scholar 

  • Fortier L, Tourdot-Maréchal R, Diviès C, Lee B, Guzzo J (2003) Induction of Oenococcus oeni H+-ATPase activity and mRNA transcription under acidic conditions. FEMS Microbiol Lett 222:165–169

    Article  CAS  PubMed  Google Scholar 

  • Garbay S, Lonvaud-Funel A (1996) Response of Leuconostoc oenos to environmental changes. J Appl Bacteriol 81:619–625

    Google Scholar 

  • Garcia-Ruiz A, Bartolomé B, Cueva C, Martin-Alvarez PJ, Moreno-Arribas MV (2009) Inactivation of oenological lactic acid bacteria (Lactobacillus hilgardii and Pediococcus pentosaceus) by phenolic compounds. J Appl Microbiol 107:1042–1053

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Ruiz A, Moreno-Arribas MV, Martin-Alvarez PJ, Bartolomé B (2011) Comparative study of the inhibitory effects of wine polyphenols on the growth of oenological lactic acid bacteria. Int J Food Microbiol 145:426–431

    Article  CAS  PubMed  Google Scholar 

  • Garvie EI (1967) The growth factor and amino acid requirements of species of the genus Leuconostoc, including Leuconostoc paramesenteroides (sp nov) and Leuconostoc oenos. J Gen Microbiol 48:439–447

    Article  CAS  PubMed  Google Scholar 

  • Gottesman S, Wickner S, Maurizi MR (1997) Protein quality control: triage by chaperones and proteases. Genes Dev 11:815–823

    Article  CAS  PubMed  Google Scholar 

  • Grandvalet C, Assad-Garcia J, Chu-Ky S, Tollot M, 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 complementation. Microbiology 154:2611–2619

    Article  CAS  PubMed  Google Scholar 

  • Guerrini S, Bastianini A, Granchi L, Vincenzini M (2002) Effect of oleic acid on Oenococcus oeni strains and Malolactic fermentation in wine. Curr Microbiol 44:5–9

    Article  CAS  PubMed  Google Scholar 

  • Guilloux-Benatier M, Le Fur Y, Feuillat M (1998) Influence of fatty acids on the growth of wine microorganisms Saccharomyces cerevisiae and Oenococcus oeni. J Ind Microbiol Biotechnol 20:144–149

    Article  CAS  Google Scholar 

  • Guilloux-Benatier M, Pageault O, Man A, Feuillat M (2000) Lysis of yeast cells by Oenococcus oeni enzymes. J Ind Microbiol Biotechnol 25:193–197

    Article  CAS  Google Scholar 

  • Guzzo J, Cavin JF, Divies C (1994) Induction of stress protein in Leuconostoc oenos to perform direct inoculation in wines. Biotechnol Lett 16:1189–1194

    Article  CAS  Google Scholar 

  • Guzzo J, Delmas F, Pierre F, Jobin MP, Samyn B, Van Beeumen J, Cavin JF, Divies C (1997) A small heat shock protein from Leuconostoc oenos induced by multiple stresses and during stationary growth phase. Lett Appl Microbiol 24:393–396

    Article  CAS  PubMed  Google Scholar 

  • Guzzo J, Jobin MP, Divies C (1998) Increase of sulfite tolerance in Oenococcus oeni by means of acidic adaptation. FEMS Microbiol Lett 160:43–47

    Article  CAS  Google Scholar 

  • Hartke A, Bouche S, Giard JC, Benachour A, Boutibonnes P, Auffray Y (1996) The lactic acid stress response of Lactococcus lactis subsp lactis. Curr Microbiol 33:194–199

    Article  CAS  PubMed  Google Scholar 

  • Henick-Kling T (1995) Control of malo-lactic fermentation in wine: energetics, flavour modification and methods of starter culture preparation. J Appl Bacteriol 79:29S–37S

    Google Scholar 

  • Henick-Kling T, Lee TH, Nicholas DJD (1986) Characterization of the lytic activity of bacteriophages of Leuconostoc oenos isolated from wine. J Appl Bacteriol 61:525–534

    Article  CAS  Google Scholar 

  • Henick-Kling T, Sandine WE, Heatherbell DA (1989) Evaluation of malolactic bacteria isolated from Oregon wines. Appl Environ Microbiol 55:2010–2016

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jackowetz JN, Mira de Orduña R (2012) Metabolism SO2 binding compounds by Oenococcus oeni during and after malolactic fermentation in white wine. Int J Food Microbiol 155:153–157

    Article  CAS  PubMed  Google Scholar 

  • Jaomanjaka F, Ballestra P, Dols-Lafargue M, Le Marrec C (2013) Expanding the diversity of oenococcal bacteriophages: insights into a novel group based on the integrase sequence. Int J Food Microbiol 166:331–340

    Article  CAS  PubMed  Google Scholar 

  • Jobin M, Delmas F, Garmyn D, Divies C, Guzzo J (1997) Molecular characterization of the gene encoding an 18-kilodalton small heat shock protein associated with the membrane of Leuconostoc oenos. Appl Environ Microbiol 63:609–614

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones RP (1989) Biological principles for the effects of ethanol. Enzyme Microb Technol 11:130–153

    Article  CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kleerebezem M, Hugenholtz J (2003) Metabolic pathway engineering in lactic acid bacteria. Curr Opin Biotechnol 14:232–237

    Article  CAS  PubMed  Google Scholar 

  • Knoll C, Divol B, du Toit M (2008) Genetic screening of lactic acid bacteria of oenological origin for bacteriocin-encoding genes. Food Microbiol 25:983–991

    Article  CAS  PubMed  Google Scholar 

  • Koch B, Kilstrup M, Vogensen FK, Hammer K (1998) Induced levels of heat shock proteins in a dnaK mutant of Lactococcus lactis. J Bacteriol 180:3873–3881

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kot W, Neve H, Heller K, Vogensen F (2014) Bacteriophages of Leuconostoc, Oenococcus, and Weissella. Front Microbiol 5:186

    Article  PubMed  PubMed Central  Google Scholar 

  • Labarre C, Guzzo J, Cavin JF (1996) Cloning and characterization of the genes encoding the malolactic enzyme and the malate permease of Leuconostoc oenos. Appl Environ Microbiol 62:1274–1282

    CAS  PubMed  PubMed Central  Google Scholar 

  • Larsen JT, Nielsen J-C, Kramp B, Richelieu M, Bjerring P, Riisager MJ, Arneborg N, Edwards CG (2003) Impact of different strains of Saccharomyces cerevisiae on malolactic fermentation by Oenococcus oeni. Am J Enol Vitic 54:246–251

    Google Scholar 

  • Lasik M (2013) The application of malolactic fermentation process to create good-quality grape wine produced in cool-climate countries: a review. Eur Food Res Technol 237:843–850

    Article  CAS  Google Scholar 

  • Lerm E, Engelbrecht L, du Toit M (2011) Selection and characterisation of Oenococcus oeni and Lactobacillus plantarum South African wine isolates for use as malolactic fermentation starter cultures. S Afr J Enol Vitic 32:280–295

    CAS  Google Scholar 

  • Lonvaud-Funel A (1995) Microbiology of the malolactic fermentation: molecular aspects. FEMS Microbiol Lett 126:209–214

    Article  CAS  Google Scholar 

  • Lonvaud-Funel A, Joyeux A (1993) Antagonism between lactic acid bacteria of wines: inhibition of Leuconostoc oenos by Lactobacillus plantarum and Pediococcus pentosaceus. Food Microbiol 10:411–419

    Article  Google Scholar 

  • Lonvaud-Funel A, Joyeux A, Desens C (1988) Inhibition of malolactic fermentation of wines by products of yeast metabolism. J Sci Food Agric 183–191

    Google Scholar 

  • Lu Y, Rock C (2006) Transcriptional regulation of fatty acid biosynthesis in Streptococcus pneumoniae. Mol Microbiol 59:551–566

    Article  CAS  PubMed  Google Scholar 

  • Maitre M, Weidmann S, Rieu A, Fenel D, Schoehn G, Ebel C, Coves J, Guzzo J (2012) The oligomer plasticity of the small heat-shock protein Lo18 from Oenococcus oeni influences its role in both membrane stabilization and protein protection. Biochem J 444:94–104

    Article  CAS  Google Scholar 

  • Maitre M, Weidmann S, Dubois-Brissonnet F, David V, Covès J, Guzzo J (2014) Adaptation of the wine bacterium Oenococcus oeni to ethanol stress: role of the small heat shock protein Lo18 in membrane integrity. Appl Environ Microbiol 80:2973–2980

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Malherbe S, Tredoux A, Nieuwoudt H, du Toit M (2012) Comparative metabolic profiling to investigate the contribution of O. oeni MLF starter cultures to red wine composition. J Ind Microbiol Biotechnol 39:477–494

    Article  CAS  PubMed  Google Scholar 

  • Manca de Nadra MC, Farias ME, Moreno-Arribas MV, Pueyo E, Polo MC (1997) Proteolytic activity of Leuconostoc oenos: effect on proteins and polypeptides from white wine. FEMS Microbiol Lett 150:135–139

    Article  CAS  Google Scholar 

  • Manca de Nadra MC, Farias ME, Moreno-Arribas V, Pueyo E, Polo MC (1999) A proteolytic effect of Oenococcus oeni on the nitrogenous macromolecular fraction of red wine. FEMS Microbiol Lett 174:41–47

    Article  Google Scholar 

  • McDonnell G, Russell AD (1999) Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12:147–179

    CAS  PubMed  PubMed Central  Google Scholar 

  • Molina-Gutierrez A, Stippl V, Delgado A, Ganzle MG, Vogel RF (2002) In situ determination of the intracellular pH of Lactococcus lactis and Lactobacillus plantarum during pressure treatment. Appl Environ Microbiol 68:4399–4406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nedovic VA, Durieux A, Van Nedervelde L, Rosseels P, Vandegans J, Plaisant A-M, Simon J-P (2000) Continuous cider fermentation with co-immobilized yeast and Leuconostoc oenos cells. Enzyme Microb Technol 26:834–839

    Article  CAS  PubMed  Google Scholar 

  • Nehme N, Mathieu F, Taillandier P (2010) Impact of the co-culture of Saccharomyces cerevisiae and Oenococcus oeni on malolactic fermentation and partial characterization of a yeast-derived inhibitory peptidic fraction. Food Microbiol 27:150–157

    Article  CAS  PubMed  Google Scholar 

  • Nel HA, Bauer R, Wolfaardt GM, Dicks LMT (2002) Effect of bacteriocins pediocin PD-1, plantaricin 423, and nisin on biofilms of Oenococcus oeni on a stainless steel surface. Am J Enol Vitic 53:191–196

    CAS  Google Scholar 

  • Nielsen JC, Prahl C, Lonvaud-Funel A (1996) Malolactic fermentation in wine by direct inoculation with freeze-dried Leuconostoc oenos cultures. Am J Enol Vitic 47:42–48

    CAS  Google Scholar 

  • Olguin N, Champomier-Verges M, Anglade P, Baraige F, Cordero-Otero R, Bordons A, Zagorec M, Requant C (2015) Transcriptomic and proteomic analyses of Oenococcus oeni PSU-1 response to ethanol shock. Food Microbiol 51:87–95

    Article  CAS  PubMed  Google Scholar 

  • Osborne JP, Edwards CG (2007) Inhibition of malolactic fermentation by a peptide produced by Saccharomyces cerevisiae during alcoholic fermentation. Int J Food Microbiol 118:27–34

    Article  CAS  PubMed  Google Scholar 

  • Osborne JP, Mira de Orduna R, Pilone GJ, Liu SQ (2000) Acetaldehyde metabolism by wine lactic acid bacteria. FEMS Microbiol Lett 191:51–55

    Article  CAS  PubMed  Google Scholar 

  • Osborne JP, Dube Morneau A, Mira de Orduna R (2006) Degradation of free and sulfur-dioxide-bound acetaldehyde by malolactic lactic acid bacteria in white wine. J Appl Microbiol 101:474–479

    Article  CAS  PubMed  Google Scholar 

  • Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496

    Article  CAS  PubMed  Google Scholar 

  • Reguant C, Bordons A, Arola L, Rozes N (2000) Influence of phenolic compounds on the physiology of Oenococcus oeni from wine. J Appl Microbiol 88:1065–1071

    Article  CAS  PubMed  Google Scholar 

  • Reguant C, Carrete R, Constanti M, Bordons A (2005a) Population dynamics of Oenococcus oeni strains in a new winery and the effect of SO2 and yeast strain. FEMS Microbiol Lett 246:111–117

    Article  CAS  PubMed  Google Scholar 

  • Reguant C, Carreté R, Ferrer N, Bordons A (2005b) Molecular analysis of Oenococcus oeni population dynamics and the effect of aeration and temperature during alcoholic fermentation on malolactic fermentation. Int J Food Sci Technol 40:451–459

    Article  CAS  Google Scholar 

  • Rizk Z, Rayess Y, Ghanem C, Mathieu F, Taillandier P, Nehme N (2016) Impact of inhibitory peptides released by Saccharomyces cerevisiae BDX on the malolactic fermentation performed by Oenococcus oeni Vitilactic F. Int J Food Microbiol 233:90–96

    Article  CAS  PubMed  Google Scholar 

  • Remize F, Augagneur Y, Guilloux-Benatier M, Guzzo J (2005) Effect of nitrogen limitation and nature of the feed upon Oenococcus oeni metabolism and extracellular protein production. J Appl Microbiol 98:652–661

    Article  CAS  PubMed  Google Scholar 

  • Rojo-Bezares B, Sáenz Y, Zarazaga M, Torres C, Ruiz-Larrea F (2007) Antimicrobial activity of nisin against Oenococcus oeni and other wine bacteria. Int J Food Microbiol 116:32–36

    Article  CAS  PubMed  Google Scholar 

  • Rollan GC, Farias ME, Strasser De Saad AM, Manca de Nadra MC (1998) Exoprotease activity of Leuconostoc oenos in stress. J Appl Microbiol 85:219–223

    Article  CAS  Google Scholar 

  • Romano A, Trip H, Lonvaud-Funel A, Lolkema JS, Lucas PM (2012) Evidence of two functionally distinct ornithine decarboxylation systems in lactic acid bacteria. Appl Environ Microbiol 78:1953–1961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rozes N, Arola L, Bordons A (2003) Effect of phenolic compounds on the co-metabolism of citric acid and sugars by Oenococcus oeni from wine. Lett Appl Microbiol 36:337–341

    Article  CAS  PubMed  Google Scholar 

  • Ruediger G, Pardon K, Sas A, Godden P, Pollnitz A (2005) Fate of pesticides during the winemaking process in relation to malolactic fermentation. J Agric Food Chem 53:3023–3026

    Article  CAS  PubMed  Google Scholar 

  • Salema M, Capucho I, Poolman B, Romao MV, Loureiro Dias M (1996) In vitro reassembly of the malolactic fermentation pathway of Leuconostoc oenos (Oenococcus oeni). J Bacteriol 178:5537–5539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    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  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sumby K, Grbin P, Jiranek (2014) Implication of news research and technologies for malolactic fermentation in wine. Appl Microbiol Biotechnol 98:8111–8132

    Article  CAS  PubMed  Google Scholar 

  • Teixeira H, Goncalves MG, Rozes N, Ramos A, San Romao MV (2002) Lactobacillic acid accumulation in the plasma membrane of Oenococcus oeni: a response to ethanol stress? Microb Ecol 43:146–153

    Article  CAS  PubMed  Google Scholar 

  • Testa B, Lombardi SJ, Tremonte P, Succi M, Tipaldi L, Pannella G, Sorrentino E, Iorizzo M, Coppola R (2014) Biodiversity of Lactobacillus plantarum from traditional italian wines. World J Microbiol Biotechnol 30:2299–2305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tourdot-Marechal 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 178:319–326

    Article  CAS  PubMed  Google Scholar 

  • Tourdot-Marechal R, Gaboriau D, Beney L, Diviès C (2000) Membrane fluidity of stressed cells of Oenococcus oeni. Int J Food Microbiol 55:269–273

    Article  CAS  PubMed  Google Scholar 

  • van Bokhorst-van de Veen H, Abee T, Tempelaars M, Bron PA, Kleerebezem M, Marco ML (2011) Short- and long-term adaptation to ethanol stress and its cross-protective consequences in Lactobacillus plantarum. Appl Environ Microbiol 77:5247–5256

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Versari A, Parpinello GP, Cattaneo M (1999) Leuconostoc oenos and malolactic fermentation in wine: a review. J Ind Microbiol Biotechnol 23:447–455

    Article  CAS  Google Scholar 

  • Vidal M, Poblet M, Constanti M, Bordons A (2001) Inhibitory effect of copper and dichlofluanid on Oenococcus oeni and malolactic fermentation. Am J Enol Vitic 52:3

    Google Scholar 

  • Vivas N, Lonvaud-Funel A, Glories Y (1997) Effect of phenolic acids and anthocyanins on growth, viability and malolactic activity of a lactic acid bacterium. Food Microbiol 14:291–300

    Article  CAS  Google Scholar 

  • Weber FJ, de Bont JA (1996) Adaptation mechanisms of microorganisms to the toxic effects of organic solvents on membranes. Biochim Biophys Acta 1286:225–245

    Article  CAS  PubMed  Google Scholar 

  • Wells A, Osborne JP (2011) Production of SO2 binding compounds and SO2 by Saccharomyces during alcoholic fermentation and the impact on malolactic fermentation.

    Google Scholar 

  • Wells A, Osborne JP (2012) Impact of acetaldehyde- and pyruvic acid-bound sulphur dioxide on wine lactic acid bacteria. Lett Appl Microbiol 54:187–194

    Article  CAS  PubMed  Google Scholar 

  • Yurdugül S, Bozoglu F (2002) Studies on an inhibitor produced by lactic acid bacteria of wines on the control of malolactic fermentation. Eur Food Res Technol 215:38–41

    Article  CAS  Google Scholar 

  • Zhang G, Fan M, Lv Q, Li Y, Liu Y, Zhang S, Zhang H (2013) The effect of cold, acid and ethanol shocks on synthesis of membrane fatty acid, freeze-drying survival and malolactic activity of Oenococcus oeni. Ann Microbiol 63:477–485

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut Jules Guyot, UMR A PAM Université de Bourgogne, Rue Claude Ladrey BP 27877, 21078, Dijon, France

    Jean Guzzo & Stéphanie Weidmann

  2. Nexidia SAS, 15 Rue de Mayence, 21000, Dijon, France

    Nicolas Desroche

Authors
  1. Jean Guzzo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicolas Desroche
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stéphanie Weidmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stéphanie Weidmann .

Editor information

Editors and Affiliations

  1. Institute of Microbiology and Wine Research, Johannes Gutenberg University, Mainz, Germany

    Helmut König

  2. Microbiology and Wine Research, Institute of Molecular Physiology, Johannes Gutenberg University, Mainz, Germany

    Gottfried Unden

  3. Erbslöh Geisenheim AG, Geisenheim, Germany

    Jürgen Fröhlich

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Guzzo, J., Desroche, N., Weidmann, S. (2017). 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, Cham. https://doi.org/10.1007/978-3-319-60021-5_17

Download citation

Publish with us

Policies and ethics

Search

Navigation