The Species-Specific Acquisition and Diversification of a K1-like Family of Killer Toxins in Budding Yeasts of the Saccharomycotina

Killer toxins are extracellular antifungal proteins that are produced by a wide variety of fungi, including Saccharomyces yeasts. Although many Saccharomyces killer toxins have been previously identified, their evolutionary origins remain uncertain given that many of these genes have been mobilized...

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Published in:	PLoS genetics Vol. 17; no. 2; p. e1009341
Main Authors:	Fredericks, Lance R, Lee, Mark D, Crabtree, Angela M, Boyer, Josephine M, Kizer, Emily A, Taggart, Nathan T, Roslund, Cooper R, Hunter, Samuel S, Kennedy, Courtney B, Willmore, Cody G, Tebbe, Nova M, Harris, Jade S, Brocke, Sarah N, Rowley, Paul A
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 01-02-2021 Public Library of Science (PLoS)
Subjects:	Ammonium Ammonium sulfate Ascomycota - classification Ascomycota - genetics Ascomycota - virology Biology and Life Sciences Cell culture Centrifugation Dextrose Endoplasmic reticulum Evolution, Molecular Fungi Gene Flow Gene Transfer, Horizontal Genetic Variation Killer Factors, Yeast - genetics Medicine and Health Sciences Methylene blue Peptides Peptone pH effects Phenotypes Phylogeny Proteins Replica plating Research and Analysis Methods RNA, Double-Stranded - genetics RNA, Viral - genetics Saccharomyces - classification Saccharomyces - genetics Saccharomyces - virology Saccharomyces cerevisiae - genetics Saccharomycetales - classification Saccharomycetales - genetics Saccharomycetales - virology Satellites Species Specificity Temperature Totivirus - genetics Toxins Yeast
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Summary:	Killer toxins are extracellular antifungal proteins that are produced by a wide variety of fungi, including Saccharomyces yeasts. Although many Saccharomyces killer toxins have been previously identified, their evolutionary origins remain uncertain given that many of these genes have been mobilized by double-stranded RNA (dsRNA) viruses. A survey of yeasts from the Saccharomyces genus has identified a novel killer toxin with a unique spectrum of activity produced by Saccharomyces paradoxus. The expression of this killer toxin is associated with the presence of a dsRNA totivirus and a satellite dsRNA. Genetic sequencing of the satellite dsRNA confirmed that it encodes a killer toxin with homology to the canonical ionophoric K1 toxin from Saccharomyces cerevisiae and has been named K1-like (K1L). Genomic homologs of K1L were identified in six non-Saccharomyces yeast species of the Saccharomycotina subphylum, predominantly in subtelomeric regions of the genome. When ectopically expressed in S. cerevisiae from cloned cDNAs, both K1L and its homologs can inhibit the growth of competing yeast species, confirming the discovery of a family of biologically active K1-like killer toxins. The sporadic distribution of these genes supports their acquisition by horizontal gene transfer followed by diversification. The phylogenetic relationship between K1L and its genomic homologs suggests a common ancestry and gene flow via dsRNAs and DNAs across taxonomic divisions. This appears to enable the acquisition of a diverse arsenal of killer toxins by different yeast species for potential use in niche competition.
Bibliography:	new_version Current address: University of California Davis Genome Center, University of California Davis, Davis, California, United States of America The authors have declared that no competing interests exist.
ISSN:	1553-7404 1553-7390 1553-7404
DOI:	10.1371/journal.pgen.1009341