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.
Highlights
Comparative genomics is a powerful tool for the investigation of yeast evolution[1,2]
Comparative genomics between G. candidum and other Saccharomycotina yeasts demonstrated the existence of groups of genes specific to G. candidum and greatly-amplified gene families which appear to contribute to the known phenotypic specificity of this yeast, while the significance of others, such as the large repertoire of carbohydrate hydrolases otherwise only found in filamentous fungi, can only be hypothesized
We were interested to study whether the origins of these genes present in G. candidum could be explained by horizontal gene transfers (HGT) or another mechanism, and undertook further analyses based on individual gene phylogenies
Summary
Comparative genomics is a powerful tool for the investigation of yeast evolution[1,2]. G. candidum presents unusual characteristics that have complicated its taxonomic classification It displays high morphological variability and wide phenotypic diversity, and has many features generally associated with filamentous fungi. Recent developments have shown that horizontal gene transfers (HGT) contributes to the diversity between species[34,35,36] These two gene-gain processes alone cannot account for most of the major and rapid transitions during yeast evolution such as the split between Pezizomycotina (filamentous fungi) and Saccharomycotina (yeasts) that was associated with genome contraction in the Saccharomycotina subphylum. Based on our whole genome comparisons between G. candidum and the other ascomycetes, we show that significant differential gene loss has occurred in lineages associated to major evolutionary transitions in yeasts, underscoring this evolutionary mechanism as an important force shaping genomic and functional diversity
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