Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution.

Cell type in budding yeasts is determined by the genotype at the mating-type (MAT) locus, but yeast species differ widely in their mating compatibility systems and life cycles. Among sexual yeasts, heterothallic species are those in which haploid strains fall into two distinct and stable mating types (MATa and MATα), whereas homothallic species are those that can switch mating types or that appear not to have distinct mating types [1, 2]. The evolutionary history of these mating compatibility systems is uncertain, particularly regarding the number and direction of transitions between homothallism and heterothallism, and regarding whether the process of mating-type switching had a single origin [3-5]. Here, we inferred the mating compatibility systems of 332 budding yeast species from their genome sequences. By reference to a robust phylogenomic tree [6], we detected evolutionary transitions between heterothallism and homothallism, and among different forms of homothallism. We find that mating-type switching has arisen independently at least 11 times during yeast evolution and that transitions from heterothallism to homothallism greatly outnumber transitions in the opposite direction (31 versus 3). Although the 3-locus MAT-HML-HMR mechanism of mating-type switching as seen in Saccharomyces cerevisiae had a single evolutionary origin in budding yeasts, simpler "flip/flop" mechanisms of switching evolved separately in at least 10 other groups of yeasts. These results point to the adaptive value of homothallism and mating-type switching to unicellular fungi.

Genome analysis of the yeast Diutina catenulata, a member of the Debaryomycetaceae/Metschnikowiaceae (CTG-Ser) clade.

Diutina catenulata (Candida catenulata) is an ascomycetous yeast that has been isolated from humans, animals and environmental sources. The species is a contaminant of dairy products, and has been linked to superficial and invasive infections in both humans and animals. Previous phylogenetic analyses have assigned the species to the Saccharomycetales, but failed to identify its specific clade. Here, we report the genome sequence of an environmental isolate of D. catenulata. Examination of the tRNA repertoire and coding potential of this species shows that it translates the CUG codon as serine and not leucine. In addition, two phylogenetic analyses using 204 ubiquitous gene family alignments and 3,826 single-copy genes both confirm the placement of the species in the Debaryomycetaceae/Metschnikowiaceae, or CTG-Ser clade. The sequenced isolate contains an MTLα idiomorph. However, unlike most MTL loci in related species, poly (A) polymerase (PAP) is not adjacent to MTLα1.

Evolutionary instability of CUG-Leu in the genetic code of budding yeasts.

The genetic code used in nuclear genes is almost universal, but here we report that it changed three times in parallel during the evolution of budding yeasts. All three changes were reassignments of the codon CUG, which is translated as serine (in 2 yeast clades), alanine (1 clade), or the 'universal' leucine (2 clades). The newly discovered Ser2 clade is in the final stages of a genetic code transition. Most species in this clade have genes for both a novel tRNASer(CAG) and an ancestral tRNALeu(CAG) to read CUG, but only tRNASer(CAG) is used in standard growth conditions. The coexistence of these alloacceptor tRNA genes indicates that the genetic code transition occurred via an ambiguous translation phase. We propose that the three parallel reassignments of CUG were not driven by natural selection in favor of their effects on the proteome, but by selection to eliminate the ancestral tRNALeu(CAG).