GiantGALgene clusters for the melibiose-galactose pathway inTorulaspora

Abstract

AbstractIn many yeast species the three genes at the center of the galactose catabolism pathway,GAL1,GAL10andGAL7, are neighbors in the genome and form a metabolic gene cluster. We report here that some yeast strains in the genusTorulasporahave much largerGALclusters that include genes for melibiase (MEL1), galactose permease (GAL2), glucose transporter (HGT1), phosphoglucomutase (PGM1), and the transcription factorGAL4, in addition toGAL1,GAL10, andGAL7. Together, these 8 genes encode almost all the steps in the pathway for catabolism of extracellular melibiose (a disaccharide of galactose and glucose). We show that a progenitor 5-gene cluster containingGAL 7-1-10-4-2was likely present in the common ancestor ofTorulasporaandZygotorulaspora. It addedPGM1andMEL1in the ancestor of mostTorulasporaspecies. It underwent further expansion in theT. pretoriensisclade, involving the fusion of three progenitor clusters in tandem and the gain ofHGT1. These giantGALclusters are highly polymorphic in structure, and subject to horizontal transfers, pseudogenization and gene losses. We identify recent horizontal transfers of completeGALclusters fromT. franciscaeinto one strain ofT. delbrueckii, and from a relative ofT. maleeaeinto one strain ofT. globosa. The variability and dynamic evolution ofGALclusters inTorulasporaindicates that there is strong natural selection on theGALpathway in this genus.