Killer yeasts

Killer yeasts

Killer yeasts are yeasts, such as "Saccharomyces cerevisiae", which can carry a double-stranded RNA virus, causing them to secrete a number of toxic proteins which are lethal to receptive cells.cite journal|author=Young, T. W. & Yagiu, M.|date=1978|title=A comparison of the killer character in different yeasts and its classification|journal=Antonie van Leeuwenhoek|volume=44|issue=1|pages=59-77|url=] These yeast cells are immune to the toxic effects of the protein due to an intrinsic immunity.cite journal|author=Breinig, F. Sendzik, T., Eisfeld, K. & Schmitt, M. J.|date=2006|title=Dissecting toxin immunity in virus-infected killer yeast uncovers an intrinsic strategy of self-protection |journal=PNAS |volume=103 |issue=10 |pages=3810-3815 |url=] Killer yeast strains can be a problem in commercial processing because they kill desirable strains.cite journal|author=Wickner, R.B.|year=1986|title=Double-stranded RNA replication in yeast: The killer system|journal=Annual Review of Biochemistry|volume=55|pages=pp. 373-395|url=]

RNA virus

The virus, L-A, is an icosahedral virus of "S. cerevisiae" comprising a 4.6 kb genomic segment and several satellite double-stranded RNA sequences, which are called M dsRNAs. The genomic segment encodes for the viral coat protein and a protein which replicates the viral genomes. [cite journal|author=Ribas, J. C. & Wickner, R. B.|year=1998|title=The Gag Domain of the Gag-Pol Fusion Protein Directs Incorporation into the L-A Double-stranded RNA Viral Particles in Saccharomyces cerevisiae|journal=Journal of Biological Chemistry|volume=273|issue=15|date=April 10 1998|pages=9306-9311|url=] The M dsRNAs encode the toxin, of which there are at least three variants in "S. cerevisiae",cite book|author=Wickner, R. B., Jinghua Tang, Gardner, N. A. & Johnson, J. E.|year=2008|chapter=The Yeast dsRNA Virus L-A Resembles Mammalian dsRNA Virus Cores|editor=John T. Patton|title=Segmented Double-stranded RNA Viruses: Structure and Molecular Biology|publisher=Caister Academic Press|isbn=978-1-904455-21-9|url=] and many more variants across all species.cite journal|author=Tipper, D.J. & Bostian, K.A.|year=1984|title=Double-stranded ribonucleic acid killer systems in yeasts|journal=Microbiological Reviews|volume=48|issue=2|pages=125-156|url=]

L-A is not released into the environment. It spreads between cells during yeast mating.


The initial protein product from translation of the M dsRNA is called the preprotoxin, which is targeted to the yeast secretory pathway. The preprotoxin is processed and cleaved to produce an α/β dimer, which is the active form of the toxin, and is released into the environment.cite journal|author=Bussey, H.|year=1991|title=K1 killer toxin, a pore-forming protein from yeast|journal=Molecular Microbiology|volume=5|issue=10|pages=2339-2343|url=] The two most studied variant toxins in "S. cerevisiae" are K1 and K28.

K1 binds to the β-1,6-D-glucan receptor on the target cell wall, moves inside, and then binds to the plasma membrane receptor Kre1p. It forms a cation-selective ion channel in the membrane, which is lethal to the cell.cite journal|author=Breinig, F., Tipper, D. J. & Schmitt, M. J.|year=2002|title=Kre1p, the Plasma Membrane Receptor for the Yeast K1 Viral Toxin|journal=Cell|volume=108|issue=3|pages=395-405|url=]

K28 uses the α-1,6-mannoprotein receptor to enter the cell, and utilizes the secretory pathway in reverse by displaying the endoplasmic reticulum HDEL signal. From the ER, K28 moves into the cytoplasm and shuts down DNA synthesis in the nucleus, triggering apoptosis. [cite journal|author=Reiter, J., Herker, E., Madeo, F. & Schmitt, M. J.|year=2005|title=Viral killer toxins induce caspase-mediated apoptosis in yeast|journal=Journal of Cell Biology|volume=168|issue=3|pages=353-358|url=] [cite journal|url=Eisfeld, K., Riffer, F., Mentges, J. & Schmitt, M. J.|year=2000|title=Endocytotic uptake and retrograde transport of a virally encoded killer toxin in yeast|journal=Molecular Microbiology|volume=37|issue=4|pages=926-940|url=]


Sestia, Shiha, Nikolaevaa and Goldstein (2001) claimed that K1 inhibits the TOK1 membrane potassium channel before secretion, and although the toxin reenters through the cell wall it is unable to reactivate TOK1. [cite journal|author=Sestia, F., Shiha, T. M., Nikolaevaa, N. & Goldstein, S.|year=2001|title=Immunity to K1 Killer Toxin: Internal TOK1 Blockade|journal=Cell|volume=105|issue=5|pages=637-644] However Breinig, Tipper and Schmitt (2002) showed that the TOK1 channel was not the primary receptor for K1, and that TOK1 inhibition does not confer immunity. Vališ, Mašek, Novotná, Pospíšek and Janderová (2006) experimented with mutants which produce K1 but do not have immunity to it, and suggested that cell membrane receptors were being degraded in the secretion pathway of immune cells, apparently due to the actions of unprocessed α chains. [cite journal|author=Vališ, K., Mašek, T., Novotná, D., Pospíšek, M. & Janderová, B.|year=2006|title=Immunity to killer toxin K1 is connected with the Golgi-to-vacuole protein degradation pathway|journal=Folia Microbiologica (Praha)|volume=51|issue=3|pages=196-202] [cite journal|author=Sturley, S. L., Elliot, Q, LeVitre. J. Tipper, D. J. & Bostian, K. A.|year=1986|title=Mapping of functional domains within the Saccharomyces cerevisiae type 1 killer preprotoxin|journal=The EMBO Journal|volume=5|issue=12|pages=3381-3389]

Breinig, Sendzik, Eisfeld and Schmitt (2006) showed that K28 toxin is neutralized in toxin-expressing cells by the α chain in the cytosol, which has not yet been fully processed and still contains part of a γ chain attached to the C terminus. The uncleaved α chain neutralizes the K28 toxin by forming a complex with it.

Use of toxins

The susceptibility to toxins varies greatly between yeast species and strains. Several experiments have made use of this to reliably identify strains. Morace, Archibusacci, Sestito and Polonelli (1984) used the toxins produced by 25 species of yeasts to differentiate between 112 pathogenic strains, based on their sensitivity to each toxin. [cite journal|author=Morace, G., Archibusacci, C., Sestito, M. & Polonelli, L.|year=1984|title=Strain differentiation of pathogenic yeasts by the killer system.|journal=Mycopathologia|volume=84|issue=2-3|pages=81-85] This was extended by Morace et al (1989) to use toxins to differentiate between 58 bacterial cultures.cite journal|author=Morace, G., Manzara, S., Dettori, G., Fanti, F., Conti, S., Campani, L., Polonelli, L. & Chezzi, C.|year=1989|title=Biotyping of bacterial isolates using the yeast killer system|journal=European Journal of Epidemiology|volume=5|issue=3|pages=303-310|url=] Vaughan-Martini, Cardinali and Martini (1996) used 24 strains of killer yeast from 13 species to find a resistance signature for each of 13 strains of "S. cerevisiae" used as starters in wine-making. [cite journal|author=Vaughan-Martini, A., Cardinali, G., & Martini, A.|year=1996|title=Differential killer sensitivity as a tool for fingerprinting wine-yeast strains of Saccharomyces cerevisiae|journal=Journal of Industrial Microbiology & Biotechnology|volume=17|issue=2|pages=124-127] Buzzini and Martini (2001) showed that sensitivity to toxins could be used to discriminate between 91 strains of "Candida albicans" and 223 other "Candida" strains. [cite journal|author=Buzzini, P. & Martini, A.|year=2001|title=Discrimination between Candida albicans and other pathogenic species of the genus Candida by their differential sensitivities to toxins of a panel of killer yeasts|journal=Journal of Clinical Microbiology|volume=39|issue=9|pages=3362-3364]

Others experimented with using killer yeasts to control undesirable yeasts. Palpacelli, Ciani and Rosini (1991) found that "Kluyveromyces phaffii" was effective against "Kloeckera apiculata", "Saccharomycodes ludwigii" and "Zygosaccharomyces rouxii" – all of which cause problems in the food industry. [cite journal|author=Palpacelli, V., Ciani, M. & Rosini, G.|year=1991|title=Activity of different ‘killer’ yeasts on strains of yeast species undesirable in the food industry|journal=FEMS Microbiology Letters|volume=84|issue=1|pages=75-78] Polonelli et al (1994) used a killer yeast to vaccinate against "C. albicans" in rats. [cite journal|author=Polonelli, L., De Bernardis, F., Conti, S., Boccanera, M., Gerloni, M., Morace, G. et al|year=1994|title=Idiotypic intravaginal vaccination to protect against candidal vaginitis by secretory, yeast killer toxin-like anti-idiotypic antibodies|journal=Journal of Immunology|volume=152|issue=6|pages=3175-3182] Lowes et al (2000) created a synthetic gene for the toxin HMK normally produced by "Williopsis mrakii", which they inserted into "Aspergillus niger" and showed that the engineered strain could control aerobic spoilage in maize silage and yoghurt. [cite journal|author=Lowes, K.F., Shearman, C.A., Payne, J., MacKenzie, D., Archer, D.B., Merry, R.J. & Gasson, M.J.|year=2000|title=Prevention of yeast spoilage in feed and food by the yeast mycocin HMK|journal=Applied Environmental Microbiology|volume=66|issue=3|pages=1066-1076] Ciani and Fatichenti (2001) used a toxin-producing strain of "Kluyveromyces phaffii" to control apiculate yeasts in wine-making. [cite journal|author=Ciani, M. & Fatichenti, F.|year=2001|title=Killer Toxin of Kluyveromyces phaffii DBVPG 6076 as a Biopreservative Agent to Control Apiculate Wine Yeasts|journal=Applied Environmental Microbiology|volume=67|issue=7|pages=3058-3063] Da Silvaa, Caladoa, Lucasa and Aguiar (2007) found a toxin produced by "Candida nodaensis" was effective at preventing spoilage of highly salted food by yeasts. [cite journal|author=Da Silvaa, S., Caladoa, S., Lucasa, C. & Aguiar, C.|year=2007|title=Unusual properties of the halotolerant yeast Candida nodaensis Killer toxin, CnKT|journal=Microbiol Research|volume=163|issue=2008|pages=243-251]

Several experiments suggest that antibodies that mimic the biological activity of killer toxins have application as antifungal agents. [cite journal|author=Magliani, W., Conti, S., Salati, A., Vaccari, S., Ravanetti, L., Maffei, D. L. et al|year=2004|title=Therapeutic potential of yeast killer toxin-like antibodies and mimotopes|journal=FEMS Yeast Research|volume=5|issue=1|pages=11-18]

Control methods

Young and Yagiu (1978) experimented with methods of curing killer yeasts. They found that using a cycloheximine solution at 0.05 ppm was effective in eliminating killer activity in one strain of "S. cerevisiae". Incubating the yeast at 37°C eliminated activity in another strain. The methods were not effective at reducing toxin production in other yeast species. Many toxins are sensitive to pH levels; for example K1 is permanently inactivated at pH levels over 6.5.

The greatest potential for control of killer yeasts appears to be the addition of the L-A virus and M dsRNA, or an equivalent gene, into the industrially-desirable variants of yeast, so they achieve immunity to the toxin, and also kill competing strains.


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