Multilayered horizontal operon transfers from bacteria reconstruct a thiamine salvage pathway in yeasts

Abstract

Horizontal acquisition of bacterial genes is presently recognized as an important contribution to the adaptation and evolution of eukaryotic genomes. However, the mechanisms underlying expression and consequent selection and fixation of the prokaryotic genes in the new eukaryotic setting are largely unknown. Here we show that genes composing the pathway for the synthesis of the essential vitamin B1 (thiamine) were lost in an ancestor of a yeast lineage, the Wickerhamiella/Starmerella (W/S) clade, known to harbor an unusually large number of genes of alien origin. The thiamine pathway was subsequently reassembled, at least twice, by multiple HGT events from different bacterial donors involving both single genes and entire operons. In the W/S-clade species Starmerella bombicola we obtained direct genetic evidence that all bacterial genes of the thiamine pathway are functional. The reconstructed pathway is composed by yeast and bacterial genes operating coordinately to scavenge thiamine derivatives from the environment. The adaptation of the newly acquired operons to the eukaryotic setting involved a repertoire of mechanisms until now only sparsely documented, namely longer intergenic regions, post-horizontal gene transfer (HGT) gene fusions fostering coordinated expression, gene relocation, and possibly recombination generating mosaic genes. The results provide additional evidence that HGT occurred recurrently in this yeast lineage and was crucial for the reestablishment of lost functions and that similar mechanisms are used across a broad range of eukaryotic microbes to promote adaptation of prokaryotic genes to their new environment.