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Genetic and phenotypic evidence for two groups of Oenococcus oeni strains and their prevalence during winemaking

  • Biotechnological Products and Process Engineering
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Abstract

Polymerase chain reaction (PCR)–denaturing gradient gel electrophoresis was the most relevant method to follow the diversity of lactic acid bacteria during winemaking. By targeting the rpoB gene, two types of Oenococcus oeni strains were distinguished resulting from a single mutation in the rpoB region targeted in PCR and generating two different electrophoresis profiles. The first one prevailed during fermentation and the second during ageing. Some strains of each type were isolated during winemaking and were studied using several genetic methods (real-time PCR, PCR-random amplified polymorphic DNA, multiple locus sequence typing and the presence of gene markers). Physiological characters related to environmental conditions were examined. The results confirmed the relevance of the rpoB mutation for characterising the two O. oeni subgroups. The relationship between the physiological response to stress and the rpoB genetic groups raised the question of O. oeni intraspecies grouping. A possible division within this species, of great technological interest to the wine industry, was also raised.

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References

  • Akopyanz N, Bukanov NO, Westblom TU, Kresovich S, Berg DE (1992) DNA diversity among clinical isolates of Heliobacter pylori detected by PCR-based RAPD fingerprinting. Nucleic Acids Res 20:5137–5142

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bae S, Fleet GH, Heard GM (2006) Lactic acid bacteria associated with wine grapes from several Australian vineyards. J Appl Microbiol 100:712–727

    CAS  PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 157:267–274

    CAS  PubMed  Google Scholar 

  • Chlenov M, Masuda S, Murakami KS, Nikiforov V, Darst SA, Mustaev A (2005) Structure and function of lineage-specific sequence insertions in the bacterial RNA polymerase β′ subunit. J Mol Biol 353:138–154

    CAS  PubMed  Google Scholar 

  • Claisse O, Renouf V, Lonvaud-Funel A (2007) Identification of lactic acid bacteria species based on RFLP analysis of a partial sequence of rpoB gene. J Microbiol Methods 69:387–390

    CAS  PubMed  Google Scholar 

  • Cocconcelli PS, Porro D, Galandini S, Sentini L (1995) Development of RAPD protocol for typing of strains of lactic acid bacteria and enterococci. Lett Appl Microbiol 21:376–379

    CAS  PubMed  Google Scholar 

  • Delaherche A (2006) Adaptation d’Oenococcus oeni à l’environnement oenologique, approche de génomiques comparées, trancriptomiques et protéomiques. PhD thesis. Université Bordeaux 2, France

  • 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 70:7210–7219

    PubMed  Google Scholar 

  • Derre 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

    CAS  PubMed  Google Scholar 

  • Divol B, Tonon T, Morichon S, Gindreau E, Lonvaud-Funel A (2003) Molecular characterization of Oenococcus oeni genes encoding proteins involved in arginine transport. J Appl Microbiol 94:738–746

    CAS  PubMed  Google Scholar 

  • Drancourt M, Raoult D (1999) Characterization of mutations in the rpoB gene in naturally rifampin-resistant Rickettsia species. Antimicrob Agents Chemother 43:2400–2403

    CAS  PubMed  PubMed Central  Google Scholar 

  • Enright MC, Spratt BG (1999) Multilocus sequence typing. Trends Microbiol 7:482–487

    CAS  PubMed  Google Scholar 

  • Felsentein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Gindreau E, Joyeux A, de Revel G, Claisse O, Lonvaud-Funel A (1997) Evaluation de l’établissement de levains malolactiques au sein de la microflore bactérienne indigène. J Int Sc Vigne Vin 31:197–202

    CAS  Google Scholar 

  • Jobin MP, Garmyn D, Divies C, Guzzo J (1999) Expression of the Oenococcus oeni trxA gene is induced by hydrogen peroxide and heat shock. Microbiol 145:1245–1251

    CAS  Google Scholar 

  • Jou R, Chen HY, Chiang CY, Yu MC, Su IJ (2005) Genetic diversity of multidrug-resistant Mycobacterium tuberculosis isolates and identification of 11 novel rpoB alleles in Taiwan. J Clinic Microbiol 43:1390–1394

    CAS  Google Scholar 

  • Kumar S, Tanura K, Jakobsen IB, Masatoshi N (2001) MEGA2: molecular evolutionary genetics analysis software. Arizona State University, Temple, Arizona, USA

    CAS  PubMed  Google Scholar 

  • Lechiancole T, Blaiotta G, Messina D, Fusco V, Villani F, Salzano G (2006) Evaluation of intra-specific diversities in Oenococcus oeni through analysis of genomic and expressed DNA. Syst Appl Microbiol 29:375–381

    CAS  PubMed  Google Scholar 

  • Lisitsyn NA, Sverdov ED, Moiseyeva EP, Danilevskaya ON, Nikiforov VG (1984) Mutation to rifampicin resistance at the beginning of the RNA polymerase β subunit gene in Escherichia coli. Mol Gen Genet 196:173–174

    CAS  PubMed  Google Scholar 

  • Livak KJ (1999) Allelic discrimination using fluorogenic probes and the 5′ nuclease assay. Genet Anal 14:143–149

    CAS  PubMed  Google Scholar 

  • Mathew R, Chatterji D (2006) The evolving story of the omega subunit of bacteria RNA polymerase. Trends Microbiol 14:450–455

    CAS  PubMed  Google Scholar 

  • Morse R, Collins MD, OHanlon K, Wallbanks S, Richardson PT (1996) Analysis of the β′ subunit of DNA-dependent RNA polymerase does not support the hypothesis inferred from 16S rRNA analysis that Oenococcus oeni (formerly Leuconostoc oenos) is a tachytelic (fast-evolving) bacterium. Int J Syst Bacteriol 46:1004–1009

    CAS  PubMed  Google Scholar 

  • Moschetti G, Blaiotta G, Aponte M, Catzeddu P, Villani F, Deiana P, Coppola S (1998) Random amplified polymorphic DNA and amplified ribosomal DNA spacer polymorphism: powerful methods to differentiate Streptococcus thermophilus strains. J Appl Microbiol 85:25–36

    CAS  PubMed  Google Scholar 

  • Mustaev A, Kolzov M, Markovstov V, Zaychikov E, Denissova L, Goldfarb A (1997) Molecular organization of the catalytic centre of RNA polymerase. Proc Natl Acad Sci U S A 94:6641–6645

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nanamiya H, Fugono N, Asai K, Doi RH, Kawamura F (2000) Suppression of temperature-sensitive sporulation mutation in the Bacillus subtilis sigA gene by rpoB mutation. FEMS Microbiol Lett 192:237–241

    CAS  PubMed  Google Scholar 

  • Neel MN, Lyon WR, Runft DL, Caparon M (2003) Role of the rpoB gene in growth phase expression of the SpeB cysteine protease of Streptococcus pyogenes. J Bacteriol 186:5166–5174

    Google Scholar 

  • Ovchinikov YA, Monastyrskaya GS, Gubanov VV, Guyyev SO, Salomatina IS, Shuvaeva TM, Lipkin VM, Sverdlov ED (1982) Nucleotide sequence of the rpoC gene and amino acid sequence of the β′ subunit. Nucleic Acids Res 10:4035–4044

    Google Scholar 

  • Porankiewicz J, Wang J, Clarke AK (1999) New insights into the ATP-dependent Clp protease: Escherichia coli and beyond. Mol Microbiol 32:449–458

    CAS  PubMed  Google Scholar 

  • Reguant C, Bordons A (2003) Typication of Oenococcus oeni strains by multiplex RAPD-PCR and study of population dynamics during malolactic fermentation. J Appl Microbiol 95:244–353

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Renouf V, Claisse O, Lonvaud-Funel A (2005) Numeration, identification and understanding of yeast and bacteria ecosystem on grape berry surface. Aust J Grape Wine Res 11:316–327

    Google Scholar 

  • Renouf V, Claisse O, Miot-Sertier C, Lonvaud-Funel A (2006) LAB evolution during winemaking: use of rpoB gene as a target for PCR-DGGE analysis. Food Microbiol 23:136–145

    CAS  PubMed  Google Scholar 

  • Renouf V, Claisse O, Lonvaud-Funel A (2007a) Inventory and monitoring of wine microbial consortia. Appl Microbiol Biotechnol 75:149–164

    CAS  PubMed  Google Scholar 

  • Renouf V, Delaherche A, Claisse O, Lonvaud-Funel A (2007b) Correlation between indigenous Oenococcus oeni strain resistance and the presence of genetic markers. J Ind Microbiol Biotechnol 35:27–33

    PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sato H, Yanagida F, Shinohara T, Suzuki M, Suzuki KI, Yokotsuka K (2001) Intraspecific diversity of Oenococcus oeni isolated during red wine-making in Japan. FEMS Microbiol Lett 202:109–114

    CAS  PubMed  Google Scholar 

  • Stendid J, Karlsson JO, Hogberg N (1994) Intrapsecific genetic variation in Heterbasidium annosum revealed by amplification of minisatellite DNA. Mycol Res 98:57–63

    Google Scholar 

  • Telenti A, Imboden P, Marchesi F, Lowrie D, Cole S, Colston MJ, Matter L, Schoper K, Bodmer T (1993) Detection of rifampicin-resistance mutations in Mycobacterium tuberculosis. Lancet 341:647–650

    CAS  PubMed  Google Scholar 

  • Tittawella IPP (1984) Evidence for clustering of RNA polymerase and ribosomal protein genes in six species of enterobacteria. Mol Gen Genetics 195:215–218

    CAS  Google Scholar 

  • Toulokhonov I, Artisimovitch I, Landick R (2001) Allosteric control of RNA polymerase by a site that contacts nascent RNA hairpins. Science 292:730–733

    CAS  PubMed  Google Scholar 

  • Wang GE, Wilson TJM, Jiang Q, Taylor DE (2001) Spontaneous mutations that confer antibiotic resistance in Helicobacter pylori. Antimicrob Agents Chemother 45:717–723

    Google Scholar 

  • Wibowo D, Fleet GH, Lee TH, Eschenbruch RE (1988) Factors affecting the induction of malolactic fermentation in red wines with Leuconostoc oenos. J Appl Bacteriol 64:421–428

    CAS  Google Scholar 

  • Zakharova N, Bass I, Arsenieva E, Nikiforov V, Severinov K (1998) Mutations in monoclonal antibody binding to evolutionary hypervariable region of E. coli RNA polymerase β′ subunit inhibit transcript cleavage and transcript elongation. J Biol Chem 273:19371–19374

    CAS  PubMed  Google Scholar 

  • Zapparoli G, Torriani S, Pesente P, Dellaglio F (1998) Design and evaluation of malolactic enzyme gene targeted primers for rapid identification and detection of Oenoccocus oeni in wine. Lett Appl Microbiol 27:243–246

    CAS  PubMed  Google Scholar 

Download references

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Authors and Affiliations

  1. UMR Œnologie 1219 - ISVV, 210 Chemin de Leysotte, CS 50008, 33 882, Villenave d’Ornon cedex, France

    Vincent Renouf, Lou Cadet Vayssieres, Olivier Claisse & Aline Lonvaud-Funel

  2. Laffort, BP 17, 33072, Bordeaux cedex, France

    Vincent Renouf

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  1. Vincent Renouf
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  2. Lou Cadet Vayssieres
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  3. Olivier Claisse
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  4. Aline Lonvaud-Funel
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Correspondence to Vincent Renouf.

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Renouf, V., Vayssieres, L.C., Claisse, O. et al. Genetic and phenotypic evidence for two groups of Oenococcus oeni strains and their prevalence during winemaking. Appl Microbiol Biotechnol 83, 85–97 (2009). https://doi.org/10.1007/s00253-008-1843-1

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