Skip to main content
SpringerLink
Log in

Effect of exogenous proline on the ethanolic tolerance and malolactic performance of Oenococcus oeni

  • Original Article
  • Published:
Journal of Food Science and Technology Aims and scope Submit manuscript

Abstract

The use of malolactic starter cultures, often offer no guarantee of microbiological success due to the chemical and physical factors (pH, ethanol, SO2, nutrient availability) that occur during the winemaking process. This study was born with the aim of improving the performance of the lactic acid bacteria used as a starter culture in the de-acidification of wines. Two commercial strains of Oenococcus oeni, were used. Was evaluated the effect of exogenous l-proline added during the bacterial growth, on the improvement of their survival in the presence of different ethanol concentrations and their ability to degrade l-malic acid in synthetic wine with the presence of 12% (v/v) and 13% (v/v) of ethanol. The results showed that l-proline improve ethanol tolerance and so the malolactic performances of O. oeni. This work represents an important strategy to ensure good vitality and improve the performance of the malolactic starter.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Betteridge AL, Sumby KM, Sundstrom JF, Grbin PR, Jiranek V (2018) Application of directed evolution to develop ethanol tolerant Oenococcus oeni for more efficient malolactic fermentation. Appl Microbiol Biotechnol 102:921–932

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Carillo P, Gibon Y (2011) Protocol: extraction and determination of L-proline. PrometheusWiki. Available online: https://www.researchgate.net/publication/211353600_PROTOCOL_Extraction_and_determination_of_proline. Accessed 12 Feb 2020

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Da Silveira MG, San Romão MV, 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 (7a)

    Article  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 Microb 69:5826–5832

    Article  Google Scholar 

  • De Leonardis A, Testa B, Macciola E, Lombardi SJ, Iorizzo M (2015) Exploring enzyme and microbial technology for the preparation of green table olives. Eur Food Res Technol 242:363–370

    Article  Google Scholar 

  • Hoffmann TV, Blohn C, Stanek A, Moses S, Barzantny H, Bremer E (2012) Synthesis, release, and recapture of compatible solute l-proline by osmotically stressed Bacillus subtilis cells. Appl Environ Microbiol 78:5753–5762

    Article  CAS  Google Scholar 

  • Huffer S, Clark ME, Ning JC, Blanch HW, Clark DS (2011) Role of alcohols in growth, lipid composition, and membrane fluidity of yeasts, bacteria, and archaea. Appl Environ Microb 77:6400–6408

    Article  CAS  Google Scholar 

  • Iorizzo M, Testa B, Lombardi SJ, García-Ruiz A, Muñoz-González C, Bartolomé B, Moreno-Arribas MV (2016) Selection and technological potential of Lactobacillus plantarum bacteria suitable for wine malolactic fermentation and grape aroma release. LWT-Food Sci Technol 73:557–566

    Article  CAS  Google Scholar 

  • Kumar TK, Samuel D, Jayaraman G, Srimathi T, Yu C (1998) The role of proline in the prevention of aggregation during protein folding in vitro. Biochem Mol Biol Int 46:509–517

    CAS  PubMed  Google Scholar 

  • Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19:998–1011. https://doi.org/10.1089/ars.2012.5074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu XT, Hou CL, Zhang J, Zeng XF, Qiao SY (2014) Fermentation conditions influence the fatty acid composition of the membranes of Lactobacillus reuteri I 5007 and its survival following freeze drying. Lett Appl Microbiol 59:398–403

    Article  CAS  Google Scholar 

  • Lombardi SJ, Pannella G, Iorizzo M, Moreno-Arribas MV, Tremonte P, Succi M, Sorrentino E, Macciola VD, Renzo M, Coppola R (2018) Sequential inoculum of Hanseniaspora guilliermondii and Saccharomyces cerevisiae for winemaking Campanino on an industrial scale. World J Microb Biot 34:161

    Article  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. App Environ Microbiol 80:2973–2980. https://doi.org/10.1128/aem.04178-13

    Article  Google Scholar 

  • Margalef-Català M, Araque I, Weidmann S, Guzzo J, Bordons A, Reguant C (2016) Protective role of glutathione addition against wine-related stress in Oenococcus oeni. Food Res Int 90:8–15

    Article  Google Scholar 

  • Marielle B, Sarrah G (2017) Assessment of bacterial membrane fluidity by flow cytometry. J Microbiol Meth 143:50–57

    Article  CAS  Google Scholar 

  • Martos GI, Minahk CJ, Font de Valdez G, Morero R (2007) Effects of protective agents on membrane fluidity of freeze dried Lactobacillus delbrueckii ssp. bulgaricus. Lett Appl Microbiol 45:282–288

    Article  CAS  Google Scholar 

  • Papadimitriou K, Alegría Á, De Bron PA, Angelis M, Gobbetti M, Kleerebezem M, Turroni F (2016) Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 80:837–890

    Article  CAS  Google Scholar 

  • Samuel D, Kumar TK, Ganesh G, Jayaraman G, Yang PW, Chang MM, Trivedi VD, Wang SL, Hwang KC, Chang DK, Yu C (2000) l-proline inhibits aggregation during protein refolding. Protein Sci 9:344–352

    Article  CAS  Google Scholar 

  • Silveira MG, Baumgärtner 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  Google Scholar 

  • Succi M, Pannella G, Tremonte P, Tipaldi L, Coppola R, Iorizzo M, Lombardi SJ, Sorrentino E (2017) Sub-optimal pH preadaptation improves the survival of Lactobacillus plantarum strains and the malic acid consumption in wine-like medium. Front Microbiol 8:470

    PubMed  PubMed Central  Google Scholar 

  • Takagi H, Sakai K, Morida K, Nakamori S (2000) l-proline accumulation by mutation or disruption of the l-proline oxidase gene improves resistance to freezing and desiccation stresses in Saccharomyces cerevisiae. FEMS Microbiol Lett 184:103–108

    Article  CAS  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  Google Scholar 

  • Testa B, Lombardi SJ, Macciola E, Succi M, Tremonte P, Iorizzo M (2019) Efficacy of olive leaf extract (Olea europaea L. cv Gentile di Larino) in marinated anchovies (Engraulis encrasicolus, L.) process. Heliyon 5:e01727

    Article  Google Scholar 

  • Testa B, Lombardi SJ, Iorizzo M, Letizia F, Martino C, Di Renzo M, Strollo D, Tremonte P, Pannella G, Ianiro M, Sorrentino E, Succi M, Coppola R (2020) Use of strain Hanseniaspora guilliermondii BF1 for a winemaking process of white grapes Vitis vinifera cv Fiano. Eur Food Res Technol 246:549–561. https://doi.org/10.1007/s00217-019-03424-8

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Wen-ying Z, Zhen-kui K (2013) Advanced progress on adaptive stress response of Oenococcus oeni. J Northeast Agri Univ (English Edition) 20:91–96. https://doi.org/10.1016/s1006-8104(13)60015-x

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Agricultural, Environmental and Food Sciences, University of Molise, Via De Sanctis, 86100, Campobasso, Italy

    Catello Di Martino, Bruno Testa, Francesco Letizia, Massimo Iorizzo, Silvia Jane Lombardi, Mario Ianiro, Massimo Di Renzo & Raffaele Coppola

  2. Mastroberardino SpA Winery, Atripalda, AV, Italy

    Massimo Di Renzo & Daniela Strollo

Authors
  1. Catello Di Martino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruno Testa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francesco Letizia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Massimo Iorizzo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Silvia Jane Lombardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mario Ianiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Massimo Di Renzo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Daniela Strollo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Raffaele Coppola
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Massimo Iorizzo.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Di Martino, C., Testa, B., Letizia, F. et al. Effect of exogenous proline on the ethanolic tolerance and malolactic performance of Oenococcus oeni. J Food Sci Technol 57, 3973–3979 (2020). https://doi.org/10.1007/s13197-020-04426-1

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-020-04426-1

Keywords

Search

Navigation