Insertion of Horizontally Transferred Genes within Conserved Syntenic Regions of Yeast Genomes

Abstract

Horizontal gene transfer has been occasionally mentioned in eukaryotic genomes, but such events appear much less numerous than in prokaryotes, where they play important functional and evolutionary roles. In yeasts, few independent cases have been described, some of which corresponding to major metabolic functions, but no systematic screening of horizontally transferred genes has been attempted so far. Taking advantage of the synteny conservation among five newly sequenced and annotated genomes of Saccharomycetaceae, we carried out a systematic search for HGT candidates amidst genes present in only one species within conserved synteny blocks. Out of 255 species-specific genes, we discovered 11 candidates for HGT, based on their similarity with bacterial proteins and on reconstructed phylogenies. This corresponds to a minimum of six transfer events because some horizontally acquired genes appear to rapidly duplicate in yeast genomes (e.g. YwqG genes in Kluyveromyces thermotolerans and serine recombinase genes of the IS607 family in Saccharomyces kluyveri). We show that the resulting copies are submitted to a strong functional selective pressure. The mechanisms of DNA transfer and integration are discussed, in relation with the generally small size of HGT candidates. Our results on a limited set of species expand by 50% the number of previously published HGT cases in hemiascomycetous yeasts, suggesting that this type of event is more frequent than usually thought. Our restrictive method does not exclude the possibility that additional HGT events exist. Actually, ancestral events common to several yeast species must have been overlooked, and the absence of homologs in present databases leaves open the question of the origin of the 244 remaining species-specific genes inserted within conserved synteny blocks.

Comparative genomics of protoploid Saccharomycetaceae

“…A few ''intervening'' genes correspond to horizontally transferred genes, as previously illustrated by the presence of a bacterial transposasetype of sequence in A. gossypii (Hall et al 2005). Gene transfer from bacteria to yeasts is also documented in S. kluyveri by the presence of six copies of a bacterial IS element (family IS607) on chromosomes B, G, and H (Rolland et al 2009). …”

Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus

“…Whole-genome duplication (WGD) and hybridization events also affect gene repertoire, as well-documented in yeasts (Semon and Wolfe 2007;Louis et al 2012; Morales and Dujon 2012;Marcet-Houben and Gabaldon 2015). The impact of horizontal gene transfers (HGTs), although seemingly important in Pezizomycotina, is limited in Saccharomycotina, with only a few dozen reported events so far (Rolland et al 2009;Galeote et al 2010;Marcet-Houben and Gabaldon 2010;Wisecaver et al 2014;Marsit et al 2015).…”

Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments

“…Furthermore, introgression events, defined as a relatively small region of a different species' genome found within the genome of another species and mostly occurring within the closely related species of the Saccharomyces sensu stricto group, have also been detected (Naumova et al 2005;Liti et al 2006;Doniger et al 2008;Muller and McCusker 2009a,b;Naumova et al 2011). Horizontal gene transfer, in which genes are transferred from a distantly related organism (even transkingdom) through nonsexual mechanisms, has also been described among the Saccharomyces yeasts (Hall et al 2005;Novo et al 2009;Rolland et al 2009), although it may be relatively rare.…”