Regions of low gene expression promote maintenance and adaptation of horizontally acquired genes in yeasts

We showed previously that yeasts in Starmerella and Wickerhamiella genera (W/S clade) exhibit numbers of horizontal gene transfer (HGT) events much larger than found in any other yeast species, with bacteria and other fungi (Pezizomycotina) as donors. Here we shed light on HGT in the W/S clade by carrying out the characterization of xenologous genes present in three species harboring together close to 600 xenologous genes. Metabolic genes were strongly overrepresented and either introduced functions new to yeasts or restored functions that were likely absent in the W/S clade ancestor. RNA-sequencing revealed lower global levels of expression of xenologous vs native yeast genes in two species. This difference is associated with the preferential accumulation of xenologous genes in large, AT-enriched chromosome terminal regions, dubbed “End” domains, characterized by overall lower gene expression. In one species, “End” domains were shown to be more permissive for protein diversification, but only for xenologous genes. We posit that “End” domains may generate favorable conditions for the adaptation and retention of xenologous genes, helping explain the exceptional numbers of HGT events in the W/S clade.