Skip to main content
Log in

Identification of novel GAPDH-derived antimicrobial peptides secreted by Saccharomyces cerevisiae and involved in wine microbial interactions

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Saccharomyces cerevisiae plays a primordial role in alcoholic fermentation and has a vast worldwide application in the production of fuel-ethanol, food and beverages. The dominance of S. cerevisiae over other microbial species during alcoholic fermentations has been traditionally ascribed to its higher ethanol tolerance. However, recent studies suggested that other phenomena, such as microbial interactions mediated by killer-like toxins, might play an important role. Here we show that S. cerevisiae secretes antimicrobial peptides (AMPs) during alcoholic fermentation that are active against a wide variety of wine-related yeasts (e.g. Dekkera bruxellensis) and bacteria (e.g. Oenococcus oeni). Mass spectrometry analyses revealed that these AMPs correspond to fragments of the S. cerevisiae glyceraldehyde 3-phosphate dehydrogenase (GAPDH) protein. The involvement of GAPDH-derived peptides in wine microbial interactions was further sustained by results obtained in mixed cultures performed with S. cerevisiae single mutants deleted in each of the GAPDH codifying genes (TDH1-3) and also with a S. cerevisiae mutant deleted in the YCA1 gene, which codifies the apoptosis-involved enzyme metacaspase. These findings are discussed in the context of wine microbial interactions, biopreservation potential and the role of GAPDH in the defence system of S. cerevisiae.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Albergaria H, Francisco D, Gori K, Arneborg N, Gírio F (2010) Saccharomyces cerevisiae CCMI 885 secretes peptides that inhibit the growth of some non-Saccharomyces wine-related strains. Appl Microbiol Biotechnol 86:965–972. doi:10.1007/s00253-009-2409-6

    Article  CAS  PubMed  Google Scholar 

  • Arneborg N, Siegumfeldt H, Andersen GH, Nissen P, Daria VR, Rodrigo PJ, Glückstad J (2005) Interactive optical trapping shows that confinement is a determinant of growth in a mixed yeast culture. FEMS Microbiol Lett 245:155–159. doi:10.1016/j.femsle.2005.03.008

    Article  CAS  PubMed  Google Scholar 

  • Barata A, Caldeira J, Botelheiro R, Pagliara D, Malfeito-Ferreira M, Loureiro V (2008) Survival patterns of Dekkera bruxellensis in wines and inhibitory effect of sulphur dioxide. Int J Food Microbiol 121:201–207. doi:10.1016/j.ijfoodmicro.2007.11.020

    Article  CAS  PubMed  Google Scholar 

  • Basílio ACM, Araújo PCM, Morais JOF, Silva-Filho EA, Morais MA, Simões DA (2008) Detection and identification of wild yeast contaminants of the industrial fuel ethanol fermentation process. Curr Microbiol 56:322–226. doi:10.1007/s00284-007-9085-5

    Article  PubMed  Google Scholar 

  • Bauer FF, Pretorius IS (2000) Yeast stress response and fermentation efficiency: how to survive the making of wine—a review. S Afr J Enol Vitic 21:27–51

    CAS  Google Scholar 

  • Bisson LF (1999) Stuck and sluggish fermentations. Am J Enol Vitic 50:107–119

    CAS  Google Scholar 

  • Comitini F, Ciani M (2011) Kluyveromyces wickerhamii killer toxin: purification and activity towards Brettanomyces/Dekkera yeasts in grape must. FEMS Microbiol Lett 316:77–82. doi:10.1111/j.1574-6968.2004.tb09761.x

    Article  CAS  PubMed  Google Scholar 

  • Comitini F, De JI, Pepe L, Mannazzu I, Ciani M (2004) Pichia anomala and Kluyveromyces wickerhamii killer toxins as new tools against Dekkera/Brettanomyces spoilage yeasts. FEMS Microbiol Lett 238:235–240. doi:10.1016/j.femsle.2004.07.040

  • Comitini F, Ferretti R, Clementi F, Mannuzzu 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. doi:10.1111/j.1365-2672.2005.02579.x

    Article  CAS  PubMed  Google Scholar 

  • Delgado ML, O’Connor JE, Azorin I, Renau-Piqueras J, Gil ML, Gozalbo D (2001) The glyceraldehyde-3-phosphate dehydrogenase polypeptides encoded by the Saccharomyces cerevisiae TDH1, TDH2 and TDH3 genes are also cell wall proteins. Microbiol 147:411–417

    CAS  Google Scholar 

  • Delgado ML, Gil ML, Gozalbo D (2003) Starvation and temperature upshift cause an increase in the enzymaticaly active cell wall-associated glyceraldehyde-3-phosphate dehydrogenase protein in yeast. FEMS Yeast Res 4:297–303. doi:10.1016/S1567-1356(03)00159-4

    Article  CAS  PubMed  Google Scholar 

  • Fleet GH, Heard GM (1993) Yeast growth during fermentation. In: Fleet GH (ed) Wine microbiology and biotechnology. Harwood Academic Publishers, Basel, Switzerland, pp 27–54

    Google Scholar 

  • Hansen EH, Nissen P, Sommer P, Nielsen JC, Arneborg N (2001) The effect of oxygen on the survival of non-Saccharomyces yeasts during mixed culture fermentations of grape juice with Saccharomyces cerevisiae. J Appl Microbiol 91:541–547. doi:10.1046/j.1365-2672.2001.01426.x

    Article  CAS  Google Scholar 

  • Liberal AT, Basílio ACM, Resende AM, Brasileiro BTV, Silva-Filho EA, Morais JOF, Simões DA, Morais MA (2007) Identification of Dekkera bruxellensis as a major contaminant yeast in continuous fuel ethanol fermentation. J Appl Microbiol 102:538–547. doi:10.1111/j.1365-2672.2006.03082.x

    Google Scholar 

  • Loureiro V, Malfeito-Ferreira M (2003) Spoilage yeasts in the wine industry (review). Int J Food Microbiol 86:23–50. doi:10.1016/S0168-1605(03)00246-0

    Article  CAS  PubMed  Google Scholar 

  • McAlister L, Holland MJ (1985a) Isolation and characterization of yeast strains carrying mutations in the glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 260:15013–15018

    CAS  PubMed  Google Scholar 

  • McAlister L, Holland MJ (1985b) Differential expression of the three yeast glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 260:15019–15027

    CAS  PubMed  Google Scholar 

  • Nehme N, Mathieu F, Taillandier P (2010) Impact of the co-culture of Saccharomyces cerevisiaeOenococcus oeni on malolactic fermentation and partial characterization of a yeast-derived inhibitory peptidic fraction. Food Microbiol 27:150–157. doi:10.1016/j.fm.2009.09.008

    Article  CAS  PubMed  Google Scholar 

  • Nakajima H, Amano W, Kubo T, Fukuhara A, Ihara H, Azuma YT, Tajima H, Inui T, Sawa A, Takeuchi T (2009) Glyceraldehyde-3-phosphate dehydrogenase aggregate formation participates in oxidative stress-induced cell death. J Cell Biochem 284:34331–34341. doi:10.1074/jbc.M109.027698

    CAS  Google Scholar 

  • Nissen P, Arneborg N (2003) Characterization of early deaths of non-Saccharomyces yeasts in mixed cultures with Saccharomyces cerevisiae. Arch Microbiol 180:257–263. doi:10.1007/s00203-003-0585-9

    Article  CAS  PubMed  Google Scholar 

  • Nissen P, Nielsen D, Arneborg N (2003) Viable Saccharomyces cerevisiae cells at high concentrations cause early growth arrest of non-Saccharomyces yeasts in mixed cultures by a cell-cell contact-mediated mechanism. Yeast 20:331–341. doi:10.1002/yea.965

    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. doi:10.1016/j.ijfoodmicro.2007.05.007

    Article  CAS  PubMed  Google Scholar 

  • Pérez F, Ramírez M, Regodón JA (2001) Influence of killer strains of Saccharomyces cerevisiae on wine fermentation. Antonie Van Leeuwenhoek 79:393–399. doi:10.1023/A:1012034608908

    Article  PubMed  Google Scholar 

  • Pérez-Nevado F, Albergaria H, Hogg T, Gírio F (2006) Cellular death of two non-Saccharomyces wine-related yeasts during mixed fermentations with Saccharomyces cerevisiae. Int J Food Microbiol 108:336–345. doi:10.1016/j.ijfoodmicro.2005.12.012

    PubMed  Google Scholar 

  • Pretorius IS (2000) Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast 16:675–729. doi:10.1002/1097-0061(20000615)16:8<675::AID-YEA585>3.0.CO;2-B

    Article  CAS  PubMed  Google Scholar 

  • Seo J-K, Lee MJ, Go H-J, Tae Hyun Park TH, Park NG (2012) Purification and characterization of YFGAP, a GAPDH-related novel antimicrobial peptide, from the skin of yellowfin tuna, Thunnus albacores. Fish & Shellfish Immunol 33:743–752. doi:10.1016/j.fsi.2012.06.023

    Article  CAS  Google Scholar 

  • Silva A, Almeida B, Sampaio-Marques B, Reis MIR, Ohlmeier S, Rodrigues F, Do Vale A, Ludovico P (2011) Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is a specific substrate of yeast metacaspase. Biochem Biophys Acta 1813:2044–2049. doi:10.1016/j.bbamcr.2011.09.010

    Article  CAS  PubMed  Google Scholar 

  • Sirover MA (2005) New nuclear functions of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in mammalian cells. J Cell Biochem 95:45–52. doi:10.1002/jcb.20399

    Article  CAS  PubMed  Google Scholar 

  • Wagener J, Schneider JJ, Baxmann S, Kalbacher H, Borelli C, Nuding S, Küchler R, Wehkamp J, Kaeser MD, Mailänder-Sanchez D, Braunsdorf C, Hube B, Schild L, Forssmann W-G, Korting H-C, Liepke C, Schaller M (2013) A peptide derived from the highly conserved protein GAPDH is involved in tissue protection by different antifungal strategies and epithelial immunomodulation. J Investigat Dermatol 133:144–153. doi:10.1038/jid.2012.254

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The present work was financed by FEDER funds through POFC-COMPETE and by national funds through Fundação para a Ciência e a Tecnologia (FCT) in the scope of project FCOMP-01-0124-FEDER-014055. M.G.A. and J.C. acknowledge the funding support from FCT (PEst-C/EQB/LA0006/2011). Patrícia Branco is the recipient of a PhD fellowship (SFRH/BD/89673/2012) funded by FCT, Portugal. We want also to thanks to Professors Isabel Sá-Correia (IST/UTL, Lisbon, Portugal), Luísa Marinho (FCUL, Lisbon, Portugal) and Paula Ludovico (ICVS/UM, Braga, Portugal) for kindly providing some mutant strains.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Helena Albergaria.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 84 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Branco, P., Francisco, D., Chambon, C. et al. Identification of novel GAPDH-derived antimicrobial peptides secreted by Saccharomyces cerevisiae and involved in wine microbial interactions. Appl Microbiol Biotechnol 98, 843–853 (2014). https://doi.org/10.1007/s00253-013-5411-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-5411-y

Keywords

Navigation