Evolutionary Capture of Viral and Plasmid DNA by Yeast Nuclear Chromosomes

Abstract

A 10-kb region of the nuclear genome of the yeast Vanderwaltozyma polyspora contains an unusual cluster of five pseudogenes homologous to five different genes from yeast killer viruses, killer plasmids, the 2m plasmid, and a Penicillium virus. By further database searches, we show that this phenomenon is not unique to V. polyspora but that about 40% of the sequenced genomes of Saccharomycotina species contain integrated copies of genes from DNA plasmids or RNA viruses. We propose the name NUPAVs (nuclear sequences of plasmid and viral origin) for these objects, by analogy to NUMTs (nuclear copies of mitochondrial DNA) and NUPTs (nuclear copies of plastid DNA, in plants) of organellar origin. Although most of the NUPAVs are pseudogenes, one intact and active gene that was formed in this way is the KHS1 chromosomal killer locus of Saccharomyces cerevisiae. We show that KHS1 is a NUPAV related to M2 killer virus double-stranded RNA. Many NUPAVs are located beside tRNA genes, and some contain sequences from a mixture of different extrachromosomal sources. We propose that NUPAVs are sequences that were captured by the nuclear genome during the repair of double-strand breaks that occurred during evolution and that some of their properties may be explained by repeated breakage at fragile chromosomal sites.It is well known that the nuclear genomes of most eukaryotes contain integrated fragments of organellar DNA called NUMTs (nuclear copies of mitochondrial DNA) and NUPTs (nuclear copies of plastid DNA, in plants) (26,29,44,45,57). These fragments are usually pseudogenes, although some NUMTs and NUPTs have become incorporated into functional nuclear genes (38). The NUMTs present in the nuclear genomes of Saccharomycotina yeast species were recently analyzed by Sacerdot et al. (48).In addition to their mitochondrial genomes, yeast species contain a variety of other extranuclear DNA and RNA elements, including viruses and plasmids. These extrachromosomal elements are usually considered to be autonomous entities that do not interact with nuclear DNA. When our laboratory sequenced the genome of the yeast Vanderwaltozyma polyspora (synonym: Kluyveromyces polysporus) (49), we were therefore surprised to find the genomic region we describe here, which contains integrated fragments of several plasmid-and virus-like sequences. We propose that this region was formed by the capture of plasmid and viral sequences by the same mechanism that captures mitochondrial DNA to form NUMTs (43, 65). In a literature search, we could find only one previous report of a similar finding: Utatsu et al. (59) reported the sequences of two regions of nuclear DNA from Zygosaccharomyces rouxii that were highly similar to parts of the 2m-like plasmid pSR1 from that species, but rearranged.Before describing the V. polyspora region, and similar regions found in other species, we will first briefly introduce the extrachromosomal RNA and DNA entities that are known to exist in yeasts. Extrachromosomal nucleic acids are relatively uncommon in yeasts: a broad...

Widespread Horizontal Gene Transfer from Double-Stranded RNA Viruses to Eukaryotic Nuclear Genomes

“…Transfer from nonretroviral RNA viruses to cells is thought to be extremely rare (5,19). However, several very recent cases of eukaryotes in which nonretroviral integrated RNA viruses (NIRVs) were detected (17,27,36,60,61) suggest that transfer from nonretroviral RNA viruses to cells might be much more common than previously thought. In the present study, we analyzed eukaryotic genome databases for the presence of dsRNA virus-related sequences, and we present evidence that totiviral and partitiviral genes are transferred frequently into the nuclear genomes of eukaryotes and that some transferred genes even have functions in the recipient genomes.…”

Selfish genetic elements, genetic conflict, and evolutionary innovation

“…Dramatic examples of PSDs are the killer plasmids of bacteria and yeast (63). In killer plasmids, the longer persistence of the encoded toxin relative to the antidote protein ensures that daughter cells die if the plasmid is lost.…”

“…PSDs may have been co-opted by bacterial and yeast genomes for defense against competitors, viral protection, or other phenotypes. For example, killer plasmids share some features with bacteriocins in bacteria and diffusible killer toxins in yeast, which can act to kill competitor cells lacking the linked modification-rescue mechanism (63). Bacteriocins typically produce diffusible toxins, however, and therefore target different cell lineages.…”

“…Nevertheless, some bacteriocin systems may have PSD features and may have originated from PSD plasmids in some cases. Frank and Wolfe (63) have found the evolutionary addition of killer plasmid and killer virus DNA into yeast chromosomes, contributing to "killer chromosome" genotypes that produce diffusible substances targeting competitor cell lineages.…”

Evolutionary Role of Interspecies Hybridization and Genetic Exchanges in Yeasts

“…In this case, a 10-kb chromosomal segment flanking a tRNA gene in a conserved syntenic region was found to contain 5 pseudogenes homologous in sequence to plasmid and viral genes from fungi. Subsequently, a systematic search within yeast and fungal genome sequences from public databases, using sequences of known extrachromosomal elements as queries, revealed that 42% of Saccharomycotina species (11 of 26 species tested) contain fragments of plasmid or viral origin (designated NUPAVs) integrated into their chromosomes (53). Most NUPAVs are pseudogenes, although one active gene, KHS1, encoding a killer factor, was also found in S. cerevisiae.…”