Skip to main content
SpringerLink
Log in

Phages of Yeast and Bacteria

  • Chapter
Biology of Microorganisms on Grapes, in Must and in Wine

Toxin-secreting killer yeasts of a great variety of genera including Saccharomyces, Hanseniaspora and Zygosaccharomyces are not only frequently present on grapes, they often also cause severe stuck fermentations. Since virus-infected killer strains of the wine yeast Saccharomyces cerevisiae are best studied among killer yeasts, the present chapter will summarize the most recent advances in killer yeast biology with special emphasis on yeast virology, killer toxin action and toxin immunity.

Although still controversial, phage attack on wine bacterial strains may be a source of malolactic failure during winemaking. This possibility opened the way to the characterization of phages infecting Oenococcus oeni. Molecular biology studies have centered on phage genes involved in prophage integration and on the determinants of lysis. Multiple tRNA genes appear to be targets of prophage integration in Oenococcus. Molecular studies also revealed that peptidoglycan hydrolases of phage origin may be endowed with secretion signals, a feature previously undescribed for bacteriophage endolysins.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Ackermann HW (2005). Bacteriophage classification. In Bacteriophages, Biology and Applications. Eds Kutter E, Sulakvelidze A, pp 67–89. CRC Press, Boca Raton, FL

    Google Scholar 

  • Ackermann HW, DuBow MS (1987). General properties of bacteriophages, Vol I. In Viruses of Prokaryotes. pp 1–292. CRC Press, Boca Raton, FL

    Google Scholar 

  • Arendt EK, Neve H, Hammes WP (1991a). Characterization of phage isolates from a phage-car-rying culture of Leoconostoc oenos 58 N. Appl. Microbiol. Biotechnol. 34:220–224

    Article  Google Scholar 

  • Arendt EK, Lonvaud A, Hammes WP (1991b). Lysogeny in Leuconostoc oenos. J. Gen. Microbiol. 137:2135–2139

    CAS  Google Scholar 

  • Arendt EK, Hammes WP (1992). Isolation and characterization of Leuconostoc oenos phages from German wines. Appl. Microbiol. Rev. 37:643–646

    CAS  Google Scholar 

  • Bazinet C, King J (1985). The DNA translocation vertex of dsDNA bacteriophage. Ann. Rev. Microbiol. 39:109–129

    Article  CAS  Google Scholar 

  • Becker A, Murialdo H (1990). Bacteriophage lambda DNA: the beginning of the end. J. Bacteriol. 172:2819–2924

    PubMed  CAS  Google Scholar 

  • Bevan EA, Makower M (1963). The physiological basis of the killer character in yeast. Proc. Int. Congr. Genet. 1:202–203

    Google Scholar 

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

    CAS  Google Scholar 

  • Bradley DE (1967). Ultrastructure of bacteriophages and bacteriocins. Bacteriol. Rev. 31:230–314

    PubMed  CAS  Google Scholar 

  • 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. U S A 103:3810–3815

    Article  PubMed  CAS  Google Scholar 

  • Bruenn JA (2005). The Ustilago maydis killer toxins. In Microbial Protein Toxins. Eds Schmitt MJ, Schaffrath R, pp 157–174. Springer, Berlin, Heidelberg

    Google Scholar 

  • Brüssow H, Desiere F (2001). Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol. Microbiol. 39:213–222

    Article  PubMed  Google Scholar 

  • Bussey H (1981). Physiology of killer factor in yeast. Adv. Microb. Physiol. 22:93–122

    Article  PubMed  CAS  Google Scholar 

  • Campbell AM (1962). Episomes. Adv. Genet. 11:101–146

    Google Scholar 

  • Carrau FM, Neirotti EN, Giogia O (1993). Stuck wine fermentation: effect of killer/sensitive yeast interactions. J. Ferment. Bioeng. 76:67–69

    Article  CAS  Google Scholar 

  • Cavin JF, Prevost H, Divies C (1991). Prophage curing in Leuconostoc oenos by mitomycin C induction. Am. J. Enol. Vitic. 42:163–166

    CAS  Google Scholar 

  • Ciani M, Fatichenti F (2001). Killer toxin of Kluyveromyces phaffii DBVPG 6076 as a biop-reservative agent to control apiculate wine yeasts. Appl. Environ. Microbiol. 67:3058–3063

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Davis CR, Silveira NFA, Fleet GH (1985). Occurrence and properties of bacteriophages of Leuconostoc oenos in Australian wines. Appl. Environ. Microbiol. 50:872–876

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Duda RL, Martincic K, Hendrix R (1995). Genetic basis of bacteriophage HK97 prohead assembly. J. Mol. Biol. 247:636–647

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • El-Sherbeini M, Bostian KA (1987). Viruses in fungi: infection of yeast with the K1 and K2 killer virus. Proc. Natl Acad. Sci. U S A 84:4293–4297

    Article  PubMed  CAS  Google Scholar 

  • Everson TC (1991). Control of phage in dairy plant. Bull. Int. Dairy Fed. 263:24–28

    Google Scholar 

  • Feiss M (1986). Terminase and the recognition, cutting and packaging of lambda chromosomes. Trends Genet. 2:100–104

    Article  CAS  Google Scholar 

  • 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 10 MC. FEMS Microbiol. Lett. 147:279–285

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Gleason FK, Holmgren A (1988). Thioredoxin and related proteins in prokaryotes. FEMS Microbiol. Rev. 4:271–297

    PubMed  CAS  Google Scholar 

  • Gnaegi F, Sozzi T (1983). Les bacteriophages de Leuconostoc oenos et leur importance oenologique. Bull. de L'O.I.V. 627:352–357

    Google Scholar 

  • 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. Arbor. Hort. 16:59–65

    CAS  Google Scholar 

  • Golubev WI (2006). Antagonistic interactions among yeasts. In The Yeast Handbook. Biodiversity and Ecophysiology of Yeasts. Eds Rosa CA, Peter G, pp 197–219. Springer, Berlin

    Chapter  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hendrix RW, Duda RL (1998). Bacteriophage HK97 head assembly: a protein ballet. Adv. Virus Res. 50:235–288

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Henick-Kling T, Lee TH, Nicholas DJD (1986b). Characterization of the lytic activity of bacteri-ophages of Leuconostoc oenos isolated from wine. J. Appl. Bacteriol. 61:525–534

    CAS  Google Scholar 

  • Ivanovska J, Hardwick JM (2005). Viruses activate a genetically conserved cell death pathway in a unicellular organism. J. Cell Biol. 170:391–399

    Article  PubMed  CAS  Google Scholar 

  • Jacobs CJ, Van Vuuren HJJ (1991). Effects of different killer yeasts on wine fermentations. Am. J. Enol. Vitic. 42:295–300

    CAS  Google Scholar 

  • 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 bacteri-ophages. J. Mol. Biol. 299:27–51

    Article  PubMed  CAS  Google Scholar 

  • Kakikawa M, Yokoi KJ, Kimoto H, Nakano M, Kawasaki K, Taketo A, Kodaira K (2002). Molecular analysis of the lysis protein Lys encoded by Lactobacillus plantarum phage ϕg1e. Gene 299:227–234

    Article  PubMed  CAS  Google Scholar 

  • Magliani W, Conti S, Gerloni M, Bertolotti D, Polonelli L (1997). Yeast killer system. Clin. Microbiol. Rev. 10:369–400

    PubMed  CAS  Google Scholar 

  • Marquina D, Santos A, Peinado JM (2002). Biology of killer yeasts. Int. Microbiol. 5:65–71

    Article  PubMed  CAS  Google Scholar 

  • 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. U S A 87:6228–6232

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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, integra-tive and non-essential functions. Gene 226:83–93

    Article  PubMed  CAS  Google Scholar 

  • Perez F, Ramirez M, Regodon JA (2001). Influence of killer strains of Saccharomyces cerevisiae on wine fermentation. Antonie van Leeuwenhoek 79:393–399

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Radler F, Schmitt MJ (1987). Killer toxins of yeasts: Inhibitors of fermentation and their adsorption. J. Food Protect. 50:234–238

    CAS  Google Scholar 

  • Reiter J, Herker E, Madeo F, Schmitt MJ (2005). Viral killer toxins induce caspase-mediated apoptosis in yeast. J. Cell Biol. 168:353–358

    Article  PubMed  CAS  Google Scholar 

  • Sanders ME (1987). Bacteriophages of industrial importance. In Page Ecology. Eds Goyal SN, Gerba CP, Bitton G, pp 211–244. Wiley-Interscience, New York

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 Recent Research Developments in Bacteriology. Ed. Pandalai SG, pp 103–130. Research Signpost, Transworld Research Network, Trivandrum, India

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • São-José C, Nascimento J, Parreira R, Santos MA (2007). Release of progeny phages from infected cells. In Bacteriophages: Genetics and Molecular Biology. Eds Macgrath S, van Sinderen D, pp 309–336. Caister Academic Press, Norwich, UK

    Google Scholar 

  • Schmitt MJ, Breinig F (2002). The viral killer system in yeast: from molecular biology to application. FEMS Microbiol. Rev. 26:257–276

    Article  PubMed  CAS  Google Scholar 

  • Schmitt MJ, Breinig F (2006). Yeast viral killer toxins: lethality and self-protection. Nat. Rev. Microbiol. 4:212–221

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Seki T, Choi EH, Ryu D (1985). Construction of a killer wine yeast strain. Appl. Environ. Microbiol. 49:1211–1215

    PubMed  CAS  Google Scholar 

  • Shimizu K (1993). Killer yeast. In Wine Microbiology and Biotechnology. Ed. Fleet GH, pp 243–263, Harwood Academic Publishers, Newark, NJ

    Google Scholar 

  • Sozzi T, Maret R, Poulin JM (1976). Mise en evidence de bactériophages dans le vin. Experientia 32:568–569

    Article  PubMed  CAS  Google Scholar 

  • 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. Horticult. 14:17–23

    CAS  Google Scholar 

  • Stojković EA, Rothman-Denes LB (2007). Coliphage N4 N-acetylmuramidase defines a new family of murein hydrolases. J. Mol. Biol. 366:406–419

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Van Vuuren HJJ, Jacobs CJ (1992). Killer yeasts in the wine industry: a review. Am. J. Enol. Vitic. 43:119–128

    Google Scholar 

  • Van Vuuren HJJ, Wingfield BD (1986). Killer yeasts. A cause of stuck fermentations in a wine cellar. Am. J. Enol. Vitic. 7:113–118

    Google Scholar 

  • Weiler F, Schmitt MJ (2005). Zygocin — a monomeric protein toxin secreted by virus-infected Zygosaccharomyces bailii. In Microbial Protein Toxins. Eds Schmitt MJ, Schaffrath R, pp 175–187. Springer, Berlin, Heidelberg

    Google Scholar 

  • Wickner RB (1996). Double-stranded RNA viruses of Saccharomyces cerevisiae. Microbiol. Rev. 60:250–265

    PubMed  CAS  Google Scholar 

  • Xu M, Struck DK, Deanton J, Wang I-N, Young R (2004). A signal-arrest-release sequence mediates export and control of the phage P1 endolysin. Proc. Natl Acad. Sci. U S A 101:6415–6420

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Arulandu A, Struck DK, Swanson S, Sacchettini JC, Young R (2005). Dissulfide isomeri-zation after membrane release of its SAR domain activates P1 lysozyme. Science 37:113–117

    Article  CAS  Google Scholar 

  • Young TW (1987). Killer yeasts. In The Yeasts, vol. 2. Eds Rose AH, Harrison JS, pp. 131–164, Academic, London

    Google Scholar 

  • Young R, Wang I-N, Roof WD (2000). Phages will out: strategies of host cell lysis. Trends Microbiol. 8:120–128

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Instituto de Ciência Aplicada e Tecnologia, Departamento de Biologia Vegetal, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, Lisboa, 1749-016, Portugal

    Manfred J. Schmitt & Mário A. Santos

  2. Instituto de Medicina Molecular, Faculdade de Medicina, Universidade de Lisboa Av. Prof. Egas Moniz, Ed. Egas Moniz, Lisboa, 1649-028, Portugal

    Carlos São-José

Authors
  1. Manfred J. Schmitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlos São-José
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mário A. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Institute of Microbiology and Wine Research, Johannes Gutenberg-University, Becherweg 15, Mainz, 55099, Germany

    Helmut König , Gottfried Unden  & Jürgen Fröhlich ,  & 

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Schmitt, M.J., São-José, C., Santos, M.A. (2009). Phages of Yeast and Bacteria. In: König, H., Unden, G., Fröhlich, J. (eds) Biology of Microorganisms on Grapes, in Must and in Wine. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-85463-0_5

Download citation

Publish with us

Policies and ethics

Search

Navigation