Abstract:
The evolutionary history of the characters underlying the adaptation of microorganisms to food
and biotechnological uses is poorly understood. We undertook comparative genomics to investigate
evolutionary relationships of the dairy yeast Geotrichum candidum within Saccharomycotina.
Surprisingly, a remarkable proportion of genes showed discordant phylogenies, clustering
with the filamentous fungus subphylum (Pezizomycotina), rather than the yeast subphylum
(Saccharomycotina), of the Ascomycota. These genes appear not to be the result of Horizontal Gene
Transfer (HGT), but to have been specifically retained by G. candidum after the filamentous fungi–
yeasts split concomitant with the yeasts’ genome contraction. We refer to these genes as SRAGs
(Specifically Retained Ancestral Genes), having been lost by all or nearly all other yeasts, and thus
contributing to the phenotypic specificity of lineages. SRAG functions include lipases consistent
with a role in cheese making and novel endoglucanases associated with degradation of plant
material. Similar gene retention was observed in three other distantly related yeasts representative
of this ecologically diverse subphylum. The phenomenon thus appears to be widespread in the
Saccharomycotina and argues that, alongside neo-functionalization following gene duplication
and HGT, specific gene retention must be recognized as an important mechanism for generation of
biodiversity and adaptation in yeasts.
