Abstract
Stuck and sluggish fermentations are still a major problem for winemakers. While stuck fermentations can usually be characterized by high residual sugar contents at the end of the alcoholic fermentation, sluggish fermentations are accompanied by a low rate of sugar utilization. In both scenarios, malfermentations can be caused by a variety of factors, most of which lead to a decrease in the metabolism of the fermenting yeast strain, associated by a decrease in biomass production, cell viability, and/or fermentation rate (Bisson 1999). One such factor potentially causing a variety of oenological problems during wine fermentation is the production of toxic proteins, so-called killer toxins, by certain killer yeasts. Soon after the discovery of toxin-secreting killer strains in the wine yeast S. cerevisiae (Bevan and Makower 1963), it became evident that killer yeasts and killer toxins can cause severe stuck fermentations, particularly under conditions when yeast starter cultures become suppressed by wild-type killer strains present on the grapes (Bussey 1981; Young 1987; Heard and Fleet 1987; Vagnoli et al. 1993; Perez et al. 2001; Medina et al. 1997; Santos et al. 2011; de Ullivarri et al. 2014).
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ackermann HW (2005) Bacteriophage classification. In: Kutter E, Sulakvelidze A (eds) Bacteriophages, biology and applications. CRC Press, Boca Raton, pp 67–89
Ackermann HW, DuBow MS (1987) General properties of bacteriophages. In: Viruses of prokaryotes, vol 1. CRC Press, Boca Raton, pp 1–292
Arendt EK, Hammes WP (1992) Isolation and characterization of Leuconostoc oenos phages from German wines. Appl Microbiol Rev 37:643–646
Arendt EK, Neve H, Hammes WP (1990) Characterization of phage isolates from a phage-carrying culture of Leuconostoc oenos 58 N. Appl Microbiol Biotechnol 34:220–224
Arendt EK, Lonvaud A, Hammes WP (1991) Lysogeny in Leuconostoc oenos. J Gen Microbiol 137:2135–2139
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
Bazinet C, King J (1985) The DNA translocation vertex of dsDNA bacteriophage. Annu Rev Microbiol 39:109–129
Becker A, Murialdo H (1990) Bacteriophage lambda DNA: the beginning of the end. J Bacteriol 172:2819–2924
Becker B, Blum A, Gießelmann E, Dausend J, Rammo D, Müller NC, Tschacksch E, Steimer M, Spindler J, Becherer U, Rettig J, Breinig F, Schmitt MJ (2016) H/KDEL receptors mediate host cell intoxication by a viral A/B toxin in yeast. Sci Rep 6:31105. doi:10.1038/srep31105
Betteridge A, Grbin P, Jiranek V (2015) Improving Oenococcus oeni to overcome challenges of wine malolactic fermentation. Trends Biotechnol 33:547–553
Bevan EA, Makower M (1963) The physiological basis of the killer character in yeast. Proc Int Congr Genet 1:202–203
Bisson LF (1999) Stuck and sluggish fermentations. Am J Enol Vitic 50:107–119
Bon E, Delaherche A, Bilhère E, de Daruvar A, Lonvaud-Funel A, Le Marrec C (2009) Oenococcus oeni genome plasticity is associated with fitness. Appl Environ Microbiol 75:2079–2090
Borneman AR, McCarthy JM, Chambers PJ, Bartowsky EJ (2012) Comparative analysis of the Oenococcus oeni pan genome reveals genetic diversity in industrially-relevant pathways. BMC Genomics 13:373–385
Bradley DE (1967) Ultrastructure of bacteriophages and bacteriocins. Bacteriol Rev 31:230–314
Breinig F, Sendzik T, Eisfeld K, Schmitt MJ (2006) Dissecting toxin immunity in virus-infected killer yeast uncovers an intrinsic strategy of self-protection. Proc Natl Acad Sci USA 103:3810–3815
Bruenn JA (2005) The Ustilago maydis killer toxins. In: Schmitt MJ, Schaffrath R (eds) Microbial protein toxins. Springer, Berlin, pp 157–174
Brüssow H, Desiere F (2001) Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol Microbiol 39:213–222
Bussey H (1981) Physiology of killer factor in yeast. Adv Microb Physiol 22:93–122
Campbell AM (1962) Episomes. Adv Genet 11:101–146
Carrau FM, Neirotti EN, Giogia O (1993) Stuck wine fermentation: effect of killer/sensitive yeast interactions. J Ferment Bioeng 76:67–69
Catalão MJ, Gil F, Moniz-Pereira J, São-José C, Pimentel M (2013) Diversity in bacterial lysis systems: bacteriophages show the way. FEMS Microbiol Rev 37:554–571
Cavin JF, Prevost H, Divies C (1991) Prophage curing in Leuconostoc oenos by mitomycin C induction. Am J Enol Vitic 42:163–166
Ciani M, Fatichenti F (2001) Killer toxin of Kluyveromyces phaffii DBVPG 6076 as a biopreservative agent to control apiculate wine yeasts. Appl Environ Microbiol 67:3058–3063
Comitini F, Ingeniis De J, Pep 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
Dalgaard JZ, Klar AJ, Moser MJ, Holley WR, Chatterjee A, Mian IS (1997) Statistical modeling and analysis of the LAGLIDADG family of site-specific endonucleases and identification of an intein that encodes a site-specific endonuclease of the HNH family. Nucleic Acids Res 25:4626–4638
Davis CR, Silveira NFA, Fleet GH (1985) Occurrence and properties of bacteriophages of Leuconostoc oenos in Australian wines. Appl Environ Microbiol 50:872–876
de Ullivarri MF, Mendoza LM, Raya RR (2014) Killer activity of Saccharomyces cerevisiae strains: partial characterization and strategies to improve the biocontrol efficacy in winemaking. Antonie Van Leeuwenhoek 106:865–878
Desiere F, McShan WM, van Sinderen D, Ferretti JJ, Brüssow H (2001) Comparative genomics reveals close genetic relationships between phages from dairy bacteria and pathogenic streptococci: evolutionary implications for prophage-host interactions. Virology 288:325–341
Doria F, Napoli C, Costantini A, Berta G, Saiz J-C, Garcia-Moruno E (2013) Development of a new method for detection and identification of Oenococcus oeni bacteriophages based on endolysin gene sequence and randomly amplified polymorphic DNA. Appl Environ Microbiol 79:4799–4805
Du Toit M, Pretorius IS (2000) Microbial spoilage and preservation of wine: using weapons from nature’s own arsenal – a review. S Afr J Enol Vitic 21:74–96
Duda RL, Martincic K, Hendrix R (1995) Genetic basis of bacteriophage HK97 prohead assembly. J Mol Biol 247:636–647
Eisfeld K, Riffer F, Mentges J, Schmitt MJ (2000) Endocytotic uptake and retrograde transport of a virally encoded killer toxin in yeast. Mol Microbiol 37:926–940
El-Sherbeini M, Bostian KA (1987) Viruses in fungi: infection of yeast with the K1 and K2 killer virus. Proc Natl Acad Sci USA 84:4293–4297
Everson TC (1991) Control of phage in dairy plant. Bull Int Dairy Fed 263:24–28
Feiss M (1986) Terminase and the recognition, cutting and packaging of lambda chromosomes. Trends Genet 2:100–104
Fernandes S, São-José C (2016) More than a hole: the holing lethal function may be required to fully sensitize bacteria to the lytic action of canonical endolysins. Mol Microbiol 102:92–106. doi:10.1111/mmi.13448
Garneau JE, Moineau S (2011) Bacteriophages of lactic acid bacteria and their impact on milk fermentations. Microb Cell Fact 10:S20
Gindreau E, Lonvaud-Funel A (1999) Molecular analysis of the region encoding the lytic system from Oenococcus oeni temperate bacteriophage ϕ10 MC. FEMS Microbiol Lett 171:231–238
Gindreau E, Turlois S, Lonvaud-Funel A (1997) Identification and sequence analysis of the region encoding the site-specific integration system from Leuconostoc oenos (Oenococcus oeni) temperate bacteriophage 10MC. FEMS Microbiol Lett 147:279–285
Gleason FK, Holmgren A (1988) Thioredoxin and related proteins in prokaryotes. FEMS Microbiol Rev 4:271–297
Gnaegi F, Sozzi T (1983) Les bacteriophages de Leuconostoc oenos et leur importance oenologique. Bull OIV 627:352–357
Gnaegi F, Cazelles O, Sozzi TN, D’Amico (1984) Connaissances sur les bacteriophages the Leuconostoc oenos et progrès dans la maîtrise de la fermentation malolactique des vins. Rev Suisse Vitic Arboric Hortic 16:59–65
Golubev WI (2006) Antagonistic interactions among yeasts. In: Rosa CA, Peter G (eds) The yeast handbook. Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 197–219
Heard GM, Fleet GH (1987) Occurrence and growth of killer yeasts during wine fermentation. Appl Environ Microbiol 53:2171–2174
Heiligenstein S, Eisfeld K, Sendzik T, Jimenez-Becker N, Breinig F, Schmitt MJ (2006) Retrotranslocation of a viral A/B toxin from the yeast endoplasmic reticulum is independent of ubiquitination and ERAD. EMBO J 25:4717–4727
Hendrix RW, Duda RL (1998) Bacteriophage HK97 head assembly: a protein ballet. Adv Virus Res 50:235–288
Henick-Kling T (1993) Malolactic fermentation. In: Fleet GH (ed) Wine microbiology and biotechnology. Harwood Academic, Amsterdam, pp 289–326
Henick-Kling T, Lee TH, Nicholas DJD (1986a) Inhibition of bacterial growth and malolactic fermentation in wine by bacteriophage. J Appl Bacteriol 61:287–293
Henick-Kling T, Lee TH, Nicholas DJD (1986b) Characterization of the lytic activity of bacteriophages of Leuconostoc oenos isolated from wine. J Appl Bacteriol 61:525–534
Ivanovska J, Hardwick JM (2005) Viruses activate a genetically conserved cell death pathway in a unicellular organism. J Cell Biol 170:391–399
Jacobs CJ, Van Vuuren HJJ (1991) Effects of different killer yeasts on wine fermentations. Am J Enol Vitic 42:295–300
Jaomanjaka F, Ballestra P, Dols-Lafargue M, LeMarrec C (2013) Expanding the diversity of oenococcal bacteriophages: insights in to a novel group based on the integrase sequence. Int J Food Microbiol 166:331–340
Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, Hendrix R (2000) Genomic sequences of bacteriophage HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299:27–51
Magliani W, Conti S, Gerloni M, Bertolotti D, Polonelli L (1997) Yeast killer system. Clin Microbiol Rev 10:369–400
Mahony J, van Sinderen D (2015) Novel strategies to prevent or exploit phages in fermentations, insights from phage-host interactions. Curr Opin Biotechnol 32:8–13
Marquina D, Santos A, Peinado JM (2002) Biology of killer yeasts. Int Microbiol 5:65–71
Martinac B, Zhu H, Kubalski A, Zhou XL, Culbertson M, Bussey H, Kung C (1990) Yeast K1 killer toxin forms ion channels in sensitive yeast spheroplasts and in artificial liposomes. Proc Natl Acad Sci USA 87:6228–6232
Medina K, Carrau FM, Giogia O, Bracesco N (1997) Nitrogen availability of grape juice limits killer yeast growth and fermentation activity during mixed-culture fermentation with sensitive commercial yeast strains. Appl Environ Microbiol 63:2821–2825
Mills DA, Rawsthorne H, Parker C, Tamir D, Makarova K (2005) Genomic analysis of Oenococcus oeni PSU-1 and its relevance in winemaking. FEMS Microbiol Rev 29:465–475
Musmanno RA, Di Maggio T, Coratza G (1999) Studies on strong and weak killer phenotypes of wine yeasts: production, activity of toxin in must, and its effect in mixed culture fermentation. J Appl Microbiol 87:932–938
Nascimento JG, Guerreiro-Pereira MC, Costa SF, São-José C, Santos MA (2008) Nisin-triggered activity of Lys44, the secreted endolysin from Oenococcus oeni phage fOg44. J Bacteriol 190:457–461
Nel L, Wingfield BD, van der Meer LJ, van Vuurnen HJJ (1987) Isolation and characterization of Leuconostoc oenos bacteriophages from wine and sugarcane. FEMS Microbiol Lett 44:63–67
Oliveira H, Melo LD, Santos SB, Nóbrega FL, Ferreira EC, Cerca N, Azeredo J, Kluskens LD (2013) Molecular aspects and comparative genomics of bacteriophage endolysins. J Virol 87:4558–4570
Orentaite I, Poranen MM, Oksanen HM, Daugelavicius R, Bamford DH (2016) K2 killer toxin-induced physiological changes in the yeast Saccharomyces cerevisiae. FEMS Yeast Res 16:fow003. doi:10.1093/femsyr/fow003
Parreira R, São-José C, Isidro A, Domingues S, Vieira G, Santos MA (1999) Gene organization in a central DNA fragment of Oenococcus oeni bacteriophage fOg44 encoding lytic, integrative and non-essential functions. Gene 226:83–93
Perez F, Ramirez M, Regodon JA (2001) Influence of killer strains of Saccharomyces cerevisiae on wine fermentation. Antonie Van Leeuwenhoek 79:393–399
Perrone B, Giacosa S, Rolle L, Cocolin L, Rantsiou K (2013) Investigation of the dominance behavior of Saccharomyces cerevisiae strains during wine fermentation. Int J Food Microbiol 165:156–162
Petering JE, Symons MR, Landgridge P, Henschke PA (1991) Determination of killer yeast activity in fermenting grape juice by using a marked Saccharomyces wine yeast strain. Appl Environ Microbiol 57:3232–3236
Pfeiffer P, Radler F (1982) Purification and characterization of extracellular and intracellular killer toxin of Saccharomyces cerevisae strain 28. J Gen Microbiol 128:2699–2706
Poblet-Icart M, Bordons A, Lonvaud-Funel A (1998) Lysogeny of Oenococcus oeni (syn. Leuconostoc oenos) and study of their induced bacteriophages. Curr Microbiol 36:365–369
Radler F, Schmitt MJ (1987) Killer toxins of yeasts: inhibitors of fermentation and their adsorption. J Food Prot 50:234–238
Ramos JL, Martínez-Bueno M, Molina-Henares AJ, Terán W, Watanabe K, Zhang X, Gallegos MT, Brennan R, Tobes R (2005) The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 69:326–356
Reiter J, Herker E, Madeo F, Schmitt MJ (2005) Viral killer toxins induce caspase-mediated apoptosis in yeast. J Cell Biol 168:353–358
Rodríguez-Cousino N, Maqueda M, Ambrona J, Zamora E, Esteban R, Ramírez M (2011) A new wine Saccharomyces cerevisiae killer toxin (Klus), encoded by a double-stranded RNA virus, with broad antifungal activity is evolutionary related to a chromosomal host gene. Appl Environ Microbiol 77:1822–1832
Samson JE, Moineau S (2013) Bacteriophages in food fermentations: new frontiers in a continuous arms race. Annu Rev Food Sci Technol 4:347–368
Sanders ME (1987) Bacteriophages of industrial importance. In: Goyal SN, Gerba CP, Bitton G (eds) Page ecology. Wiley-Interscience, New York, pp 211–244
Santos R, Vieira G, Santos MA, Paveia H (1996) Characterization of temperate bacteriophages of Leuconostoc oenos and evidence for two prophage attachment sites in the genome of starter strain PSU-1. J Appl Bacteriol 81:383–392
Santos R, São-José C, Vieira G, Paveia H, Santos MA (1998) Genome diversity in temperate bacteriophages of Oenococcus oeni. Arch Virol 143:523–536
Santos A, Navascués E, Bravo E, Marquina D (2011) Ustilago maydis killer toxin as a new tool for the biocontrol of the wine spoilage yeast Brettanomyces bruxellensis. Int J Food Microbiol 145:147–154
São-José C (2002) Genome analysis and gene expression in oenophage fOg44 – evidence for a new strategy of bacteriophage-induced host lysis. PhD thesis. University of Lisbon, Portugal
São-José C, Parreira R, Vieira G, Santos MA (2000) The N-terminal region of the Oenococcus oeni bacteriophage fOg44 lysin behaves as a bona fide signal peptide in Escherichia coli and as a cis-inhibitory element, preventing lytic activity on oenococcal cells. J Bacteriol 182:5823–5831
São-José C, Parreira R, Santos MA (2003) Triggering of host-cell lysis by double-stranded DNA bacteriophages: fundamental concepts, recent developments and emerging applications. In: Pandalai SG (ed) Recent research developments in bacteriology. Research Signpost, Transworld Research Network, Trivandrum, pp 103–130
São-José C, Santos S, Nascimento J, Brito-Maduro AG, Parreira R, Santos MA (2004) Diversity in the lysis-integration region of oenophage genomes and evidence for multiple tRNA loci, as targets for prophage integration in Oenococcus oeni. Virology 325:82–95
São-José C, Nascimento J, Parreira R, Santos MA (2007) Release of progeny phages from infected cells. In: Macgrath S, van Sinderen D (eds) Bacteriophages: genetics and molecular biology. Caister Academic, Norwich, pp 309–336
Schmitt MJ, Breinig F (2002) The viral killer system in yeast: from molecular biology to application. FEMS Microbiol Rev 26:257–276
Schmitt MJ, Breinig F (2006) Yeast viral killer toxins: lethality and self-protection. Nat Rev Microbiol 4:212–221
Schmitt MJ, Neuhausen F (1994) Killer toxin-secreting double-stranded RNA mycoviruses in the yeasts Hanseniaspora uvarum and Zygosaccharomyces bailii. J Virol 68:1765–1772
Schmitt MJ, Schernikau G (1997) Construction of a cDNA-based K1/K2/K28 triple killer strain of Saccharomyces cerevisiae. Food Technol Biotechnol 35:281–285
Seki T, Choi EH, Ryu D (1985) Construction of a killer wine yeast strain. Appl Environ Microbiol 49:1211–1215
Shimizu K (1993) Killer yeast. In: Fleet GH (ed) Wine microbiology and biotechnology. Harwood Academic, Newark, pp 243–263
Sozzi T, Maret R, Poulin JM (1976) Mise en evidence de bactériophages dans le vin. Experientia 32:568–569
Sozzi T, Gnaegi F, D’Amico N, Hose H (1982) Difficulties de fermentation malolactoque du vin dues à des bactériophages de Leuconostoc oenos. Rev Suisse Vitic Arboric Hortic 14:17–23
Sutherland M, van Vuuren HJ, Howe MM (1994) Cloning, sequence and in vitro transcription/translation analysis of a 3.2-kb EcoRI–HindIII fragment of Leuconostoc oenos bacteriophage L10. Gene 148:125–129
Tenreiro R, Santos R, Brito L, Paveia H, Vieira G, Santos MA (1993) Bacteriophages induced by mitomycin C treatment of Leuconostoc oenos strains from Portuguese wines. Lett Appl Microbiol 16:207–209
Vagnoli P, Musmanno RA, Cresti S, di Maggio T, Coratza G (1993) Occurrence of killer yeasts in spontaneous wine fermentations from the Tuscany region of Italy. Appl Environ Microbiol 59:4037–4043
Van Vuuren HJJ, Jacobs CJ (1992) Killer yeasts in the wine industry: a review. Am J Enol Vitic 43:119–128
Van Vuuren HJJ, Wingfield BD (1986) Killer yeasts. A cause of stuck fermentations in a wine cellar. Am J Enol Vitic 7:113–118
Weiler F, Schmitt MJ (2005) Zygocin – a monomeric protein toxin secreted by virus-infected Zygosaccharomyces bailii. In: Schmitt MJ, Schaffrath R (eds) Microbial protein toxins. Springer, Berlin, pp 175–187
Weinitschke S, Denger K, Cook AM, Smits TH (2007) The DUF81 protein TauE in Cupriavidus necator H16, a sulfite exporter in the metabolism of C2 sulfonates. Microbiology 153:3055–3060
Wickner RB (1996) Double-stranded RNA viruses of Saccharomyces cerevisiae. Microbiol Rev 60:250–265
Young TW (1987) Killer yeasts. In: Rose AH, Harrison JS (eds) The yeasts, vol 2. Academic, London, pp 131–164
Young R (2014) Phage lysis: three steps, three choices, one outcome. J Microbiol 52:243–258
Young R, Wang I-N, Roof WD (2000) Phages will out: strategies of host cell lysis. Trends Microbiol 8:120–128
Zé-Zé L, Tenreiro R, Brito L, Santos MA, Paveia H (1998) Physical map of the genome of Oenococcus oeni PSU-1 and localization of genetic markers. Microbiology 144:1145–1156
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
São-José, C., Santos, M.A., Schmitt, M.J. (2017). Viruses of Wine-Associated Yeasts and 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_5
Download citation
DOI: https://doi.org/10.1007/978-3-319-60021-5_5
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-60020-8
Online ISBN: 978-3-319-60021-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)