Advertisement

Relative expression of stress-related genes during acclimation at low temperature of psychrotrophic Oenococcus oeni strains from Patagonian wine

  • Nair Temis OlguínEmail author
  • Danay Valdés La Hens
  • Lucrecia Delfederico
  • Liliana Semorile
Original Paper
  • 54 Downloads

Abstract

In the present study, we evaluated the transcriptional response of four stress-related genes in three Oenococcus oeni strains after acclimation at two different temperatures. Gene expression was analyzed at time zero and after 48 h acclimation at 18 and 21 °C. After the acclimation period cells were inoculated into sterile Pinot noir wine and MLF was followed for 25 days to investigate if different acclimation temperatures could influence cell survival and MLF performance. l-malic acid consumption, population survival, and transcriptional behavior were different upon the acclimation temperature. rmlB and hsp20 genes presented a considerable increase in their expression level when strains were acclimated at 18 °C particularly in the psychrotrophic strains UNQOe19 and UNQOe4 isolated from Patagonian Pinot noir wine in comparison with the control strain (ATCC 27310). The increase in rmlB and hsp20 expression could account for the better survival of these strains in Pinot noir in comparison with the control strain. In addition, Patagonian populations acclimated at 18 °C were able to consume a higher percentage of l-malic acid in comparison with cells acclimated at 21 °C. Our results suggest that gene expression analysis of cells acclimated at sub-optimal temperatures could benefit the selection of psychrotrophic strains aimed as starter cultures.

Keywords

Acclimation Gene expression Malolactic fermentation Oenococcus oeni Psychrotrophic RT-qPCR 

Notes

Acknowledgements

This work was funded by grants from Universidad Nacional de Quilmes (Programa Microbiología Molecular Básica y Aplicada—Resolución (R) Nº 954/17); Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC-PBA, Proyecto PIT-AP-BA Nº 173/16); Consejo Interuniversitario Nacional—Consejo Nacional de Investigaciones Científicas y Técnicas (CIN—CONICET, PDTS 2014 Nº 173); and Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT, PICT 2014 Nº 1395, PICT 2017 Nº 1156). DVH and LS are members of the Research Career of CIC-BA; NTO is a member of the Research Career of CONICET.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abrahamse CE, Bartowsky EJ (2012) Timing of malolactic fermentation inoculation in Shiraz grape must and wine: influence on chemical composition. World J Microbiol Biotechnol 28:255–265.  https://doi.org/10.1007/s11274-011-0814-3 CrossRefPubMedGoogle Scholar
  2. Andersen C, Jensen J, Orntoft T (2004) Normalization of real­time quantitative reverse transcription—PCR data: a model­based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64:5245.  https://doi.org/10.1158/0008 CrossRefPubMedGoogle Scholar
  3. Antalick G, Perello MC, De Revel G (2013) Co-inoculation with yeast and LAB under winery conditions: modification of the aromatic profile of Merlot wines. South Afr J Enol Vitic 34:223–232Google Scholar
  4. Bartowsky EJ (2005) Oenococcus oeni and malolactic fermentation–moving into the molecular arena. Aust J Grape Wine Res 11:174–187.  https://doi.org/10.1111/j.1755-0238.2005.tb00286.x CrossRefGoogle Scholar
  5. Bartowsky EJ, Borneman AR (2011) Genomic variations of Oenococcus oeni strains and the potential to impact on malolactic fermentation and aroma compounds in wine. Appl Microbiol Biotechnol 92:441–447.  https://doi.org/10.1007/s00253-011-3546-2 CrossRefPubMedGoogle Scholar
  6. Bartowsky EJ, Henschke PA (2004) The “buttery” attribute of wine—diacetyl—desirability, spoilage and beyond. Int J Food Microbiol 96:235–252.  https://doi.org/10.1016/j.ijfoodmicro.2004.05.013 CrossRefPubMedGoogle Scholar
  7. Bartowsky EJ, Costello PJ, Chambers PJ (2015) Emerging trends in the application of malolactic fermentation. Aust J Grape Wine Res 21:663–669.  https://doi.org/10.1111/ajgw.12185 CrossRefGoogle Scholar
  8. Beltramo C, Desroche N, Tourdot-Maréchal R et al (2006) Real-time PCR for characterizing the stress response of Oenococcus oeni in a wine-like medium. Res Microbiol 157:267–274.  https://doi.org/10.1016/j.resmic.2005.07.006 CrossRefPubMedGoogle Scholar
  9. Betteridge AL, Sumby KM, Sundstrom JF et al (2018) Application of directed evolution to develop ethanol tolerant Oenococcus oeni for more efficient malolactic fermentation. Appl Microbiol Biotechnol 102:921–932.  https://doi.org/10.1007/s00253-017-8593-x CrossRefPubMedGoogle Scholar
  10. Bordas M, Araque I, Bordons A, Reguant C (2015) Differential expression of selected Oenococcus oeni genes for adaptation in wine-like media and red wine. Ann Microbiol 65:2277–2285.  https://doi.org/10.1007/s13213-015-1069-2 CrossRefGoogle Scholar
  11. Bourdineaud J, Nehme 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 Microb 69:2512–2520.  https://doi.org/10.1128/AEM.69.5.2512 CrossRefGoogle Scholar
  12. Bravo-Ferrada BM, Tymczyszyn EE, Gómez-Zavaglia A, Semorile L (2014) Effect of acclimation medium on cell viability, membrane integrity and ability to consume malic acid in synthetic wine by oenological Lactobacillus plantarum strains. J Appl Microbiol 116:360–367.  https://doi.org/10.1111/jam.12372 CrossRefPubMedGoogle Scholar
  13. Bravo-Ferrada BM, Hollmann A, Brizuela N et al (2016) Growth and consumption of l-malic acid in wine-like medium by acclimated and non-acclimated cultures of Patagonian Oenococcus oeni strains. Folia Microbiol (Praha) 61:365–373.  https://doi.org/10.1007/s12223-016-0446-y CrossRefGoogle Scholar
  14. 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.  https://doi.org/10.1111/j.1365-2672.1990.tb02544.x CrossRefGoogle Scholar
  15. Brizuela NS, Bravo-Ferrada BM, La Hens DV et al (2017) Comparative vinification assays with selected Patagonian strains of Oenococcus oeni and Lactobacillus plantarum. LWT Food Sci Technol 77:348–355.  https://doi.org/10.1016/j.lwt.2016.11.023 CrossRefGoogle Scholar
  16. Cañas PMI, Pérez PR, Prieto SS, Herreros MLP (2009) Ecological study of lactic acid microbiota isolated from Tempranillo wines of Castilla-La Mancha. J Biosci Bioeng 108:220–224.  https://doi.org/10.1016/j.jbiosc.2009.04.001 CrossRefPubMedGoogle Scholar
  17. Capozzi V, Russo P, Beneduce L et al (2010) Technological properties of Oenococcus oeni strains isolated from typical southern Italian wines. Lett Appl Microbiol 50:327–334.  https://doi.org/10.1111/j.1472-765X.2010.02795.x CrossRefPubMedGoogle Scholar
  18. Cecconi D, Milli A, Rinalducci S et al (2009) Proteomic analysis of Oenococcus oeni freeze-dried culture to assess the importance of cell acclimation to conduct malolactic fermentation in wine. Electrophoresis 30:2988–2995.  https://doi.org/10.1002/elps.200900228 CrossRefPubMedGoogle Scholar
  19. 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 1717:118–124.  https://doi.org/10.1016/j.bbamem.2005.09.015 CrossRefPubMedGoogle Scholar
  20. Costantini A, Vaudano E, Rantsiou K et al (2011) Quantitative expression analysis of mleP gene and two genes involved in the ABC transport system in Oenococcus oeni during rehydration. Appl Microbiol Biotechnol 91:1601–1609.  https://doi.org/10.1007/s00253-011-3498-6 CrossRefPubMedGoogle Scholar
  21. Costantini A, Rantsiou K, Majumder A et al (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.  https://doi.org/10.1016/j.jprot.2015.04.019 CrossRefPubMedGoogle Scholar
  22. Coucheney F, Desroche N, Bou M et al (2005) A new approach for selection of Oenococcus oeni strains in order to produce malolactic starters. Int J Food Microbiol 105:463–470.  https://doi.org/10.1016/j.ijfoodmicro.2005.04.023 CrossRefPubMedGoogle Scholar
  23. De Man JC, Rogosa M, Sharpe (1960) A medium for the cultivation of Lactobacilli. J Appl Bacteriol 23:130–135.  https://doi.org/10.1111/j.1365-2672.1960.tb00188.x CrossRefGoogle Scholar
  24. Desroche N, Beltramo C, Guzzo J (2005) Determination of an internal control to apply reverse transcription quantitative PCR to study stress response in the lactic acid bacterium Oenococcus oeni. J Microbiol Methods 60:325–333.  https://doi.org/10.1016/j.mimet.2004.10.010 CrossRefPubMedGoogle Scholar
  25. du Toit M, Engelbrecht L, Lerm E, Krieger-Weber S (2011) Lactobacillus: the next generation of malolactic fermentation starter cultures—an overview. Food Bioprocess Technol 4:876–906.  https://doi.org/10.1007/s11947-010-0448-8 CrossRefGoogle Scholar
  26. González-Arenzana L, Santamaría P, López R et al (2012) Ecology of indigenous lactic acid bacteria along different winemaking processes of Tempranillo Red Wine from La Rioja (Spain). Sci World J 2012:1–7.  https://doi.org/10.1100/2012/796327 CrossRefGoogle Scholar
  27. Guzzon R, Poznanski E, Conterno L et al (2009) Selection of a new highly resistant strain for malolactic fermentation under difficult conditions. South Afr J Enol Vitic 30:133–141Google Scholar
  28. Guzzon R, Moser S, Davide S et al (2016) Exploitation of simultaneous alcoholic and malolactic fermentation of Incrocio Manzoni, a traditional Italian white wine. South Afr J Enol Vitic 37:124–131.  https://doi.org/10.21548/37-2-828 CrossRefGoogle Scholar
  29. Iglesias NG, Valdés La Hens D, Olguin NT et al (2018) Genome sequence of Oenococcus oeni UNQOe19, the first fully assembled genome sequence of a patagonian psychrotrophic oenological strain. Microbiol Resour Announc 7:e00889-18CrossRefGoogle Scholar
  30. Lafon Lafourcade S, Carre E, Ribereau Gayon P (1983) Occurrence of lactic acid bacteria during the different stages of vinification and conservation of wines. Appl Environ Microbiol 46:874–880PubMedPubMedCentralGoogle Scholar
  31. 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.  https://doi.org/10.1007/s00217-013-2083-x CrossRefGoogle Scholar
  32. Maitre M, Weidmann S, Dubois-Brissonnet F et al (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.  https://doi.org/10.1128/AEM.04178-13 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Manera C, Bravo-Ferrada BM, Tymczyszyn E, Delfederico L, Olguín N, Semorile LC, Valdés La Hens D (2017) Aislamiento y selección de cepas psicrotolerantes de bacterias lácticas enológicas de la región patagónica. In IV Congreso Internacional Científico y Tecnológico-CONCyT. http://digital.cic.gba.gob.ar/handle/11746/6684
  34. Margalef-Català M, Araque I, Bordons A et al (2016) Transcriptomic and proteomic analysis of Oenococcus oeni adaptation to wine stress conditions. Front Microbiol.  https://doi.org/10.3389/fmicb.2016.01554 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Marques AP, Duarte AJ, Chambel L et al (2011) Genomic diversity of Oenococcus oeni from different winemaking regions of Portugal. Int Microbiol 14:155–162.  https://doi.org/10.2436/20.1501.01.144 CrossRefPubMedGoogle Scholar
  36. Marques AP, San Romão MV, Tenreiro R (2012) RNA fingerprinting analysis of Oenococcus oeni strains under wine conditions. Food Microbiol 31:238–245.  https://doi.org/10.1016/j.fm.2012.02.006 CrossRefPubMedGoogle Scholar
  37. Matthews A, Grimaldi A, Walker M et al (2004) Lactic acid bacteria as a potential source of enzymes for use in vini cation. Society 70:5715–5731.  https://doi.org/10.1128/AEM.70.10.5715 CrossRefGoogle Scholar
  38. Miranda-Castilleja DE, Martínez-Peniche R, Aldrete-Tapia JA et al (2016) Distribution of native lactic acid bacteria in wineries of Queretaro, Mexico and their resistance to wine-like conditions. Front Microbiol 7:1–9.  https://doi.org/10.3389/fmicb.2016.01769 CrossRefGoogle Scholar
  39. Nisiotou AA, Dourou D, Filippousi ME et al (2015) Genetic and technological characterisation of vineyard- and winery-associated lactic acid bacteria. Biomed Res Int.  https://doi.org/10.1155/2015/508254 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Olguín N, Bordons A, Reguant C (2009) Influence of ethanol and pH on the gene expression of the citrate pathway in Oenococcus oeni. Food Microbiol 26:197–203.  https://doi.org/10.1016/j.fm.2008.09.004 CrossRefPubMedGoogle Scholar
  41. Olguín N, Bordons A, Reguant C (2010) Multigenic expression analysis as an approach to understanding the behaviour of Oenococcus oeni in wine-like conditions. Int J Food Microbiol 144:88–95.  https://doi.org/10.1016/j.ijfoodmicro.2010.08.032 CrossRefPubMedGoogle Scholar
  42. Olguín N, Champomier-Vergès M, Anglade P et al (2015) Transcriptomic and proteomic analysis of Oenococcus oeni PSU-1 response to ethanol shock. Food Microbiol 51:87–95.  https://doi.org/10.1016/j.fm.2015.05.005 CrossRefPubMedGoogle Scholar
  43. Reguant C, Carreté R, Constantí M, Bordons A (2005) Population dynamics of Oenococcus oeni strains in a new winery and the effect of SO2 and yeast strain. FEMS Microbiol Lett 246:111–117.  https://doi.org/10.1016/j.femsle.2005.03.045 CrossRefPubMedGoogle Scholar
  44. Ribéreau-Gayon P, Glories Y, Maujean A, Dubourdieu D (2006) Handbook of enology: the microbiology of wine and vinifications. Wiley, HobokenCrossRefGoogle Scholar
  45. Ruiz P, Seseña S, Izquierdo PM, Palop ML (2010) Bacterial biodiversity and dynamics during malolactic fermentation of Tempranillo wines as determined by a culture-independent method (PCR-DGGE). Appl Microbiol Biotechnol 86:1555–1562.  https://doi.org/10.1007/s00253-010-2492-8 CrossRefPubMedGoogle Scholar
  46. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108.  https://doi.org/10.1038/nprot.2008.73 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Silveira MG, Baumgärtner M, Rombouts FM, Grac M (2004) Effect of adaptation to ethanol on cytoplasmic and membrane protein profiles of Oenococcus oeni effect of adaptation to ethanol on cytoplasmic and membrane protein profiles of Oenococcus oeni. Appl Environ Microbiol 70:2748–2755.  https://doi.org/10.1128/AEM.70.5.2748 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Sternes PR, Costello PJ, Chambers PJ et al (2017) Whole transcriptome RNAseq analysis of Oenococcus oeni reveals distinct intra-specific expression patterns during malolactic fermentation, including genes involved in diacetyl metabolism. Int J Food Microbiol 257:216–224.  https://doi.org/10.1016/j.ijfoodmicro.2017.06.024 CrossRefPubMedGoogle Scholar
  49. Tristezza M, di Feo L, Tufariello M et al (2016) Simultaneous inoculation of yeasts and lactic acid bacteria: effects on fermentation dynamics and chemical composition of Negroamaro wine. LWT Food Sci Technol 66:406–412.  https://doi.org/10.1016/j.lwt.2015.10.064 CrossRefGoogle Scholar
  50. Valdés La Hens D, Bravo-Ferrada BM, Delfederico L et al (2015) Prevalence of Lactobacillus plantarum and Oenococcus oeni during spontaneous malolactic fermentation in Patagonian red wines revealed by polymerase chain reaction-denaturing gradient gel electrophoresis with two targeted genes. Aust J Grape Wine Res 21:49–56.  https://doi.org/10.1111/ajgw.12110 CrossRefGoogle Scholar
  51. Vandesompele J, De Preter K, Pattyn F et al (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:31–34.  https://doi.org/10.1186/gb-2002-3-7-research0034 CrossRefGoogle Scholar
  52. Vigentini I, Picozzi C, Tirelli A et al (2009) Survey on indigenous Oenococcus oeni strains isolated from red wines of Valtellina, a cold climate wine-growing Italian area. Int J Food Microbiol 136:123–128.  https://doi.org/10.1016/j.ijfoodmicro.2009.09.009 CrossRefPubMedGoogle Scholar
  53. Vigentini I, Praz A, Domeneghetti D et al (2016) Characterization of malolactic bacteria isolated from Aosta Valley wines and evidence of psychrotrophy in some strains. J Appl Microbiol 120:934–945.  https://doi.org/10.1111/jam.13080 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Laboratorio de Microbiología Molecular, Instituto de Microbiología Básica y Aplicada (IMBA), Departamento de Ciencia y TecnologíaUniversidad Nacional de QuilmesBernalArgentina
  2. 2.Comisión de Investigaciones Científicas de la Provincia de Buenos Aires - CIC-BALa PlataArgentina
  3. 3.Consejo Nacional de Investigaciones Científicas y Técnicas – CONICETCiudad de Buenos AiresArgentina

Personalised recommendations