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ARS Home » Midwest Area » Peoria, Illinois » National Center for Agricultural Utilization Research » Mycotoxin Prevention and Applied Microbiology Research » Research » Publications at this Location » Publication #342243
Title: Factors driving metabolic diversity in the budding yeast subphylum

Author
item OPULENTE, DANA - University Of Wisconsin
item ROLLINSON, EMILY - Pennsylvania State University
item BERNICK-ROEHR, CLEOME - University Of Wisconsin
item HULFACHOR, AMANDA - University Of Wisconsin
item ROKAS, ANTONIS - Vanderbilt University
item Kurtzman, Cletus
item HITTINGER, CHRIS - University Of Wisconsin

Submitted to: BMC Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/13/2018
Publication Date: 3/2/2018
Citation: Opulente, D.A., Rollinson, E.J., Bernick-Roehr, C., Hulfachor, A.B., Rokas, A., Kurtzman, C.P., Hittinger, C.T. 2018. Factors driving metabolic diversity in the budding yeast subphylum. BMC Biology. 16:26. https://doi.org/10.1186/s12915-018-0498-3.
DOI: https://doi.org/10.1186/s12915-018-0498-3

Interpretive Summary: We examined the growth capabilities and genetic relatedness of yeast species to determine if only closely related species had certain unique traits or whether these traits were also shared by other distantly related yeasts. The aim of this study was to provide direction for discovery of species likely to have value for agricultural and biotechnological applications and where these species might be found in nature. The study examined 48 metabolic activities from 784 species isolated from 50 environments. It was found that closely related species often occupy the same environmental niche, but some distantly related species with similar metabolism may also have adapted to these same niches. These results indicate that specific metabolic capabilities may be found among distantly related yeasts. Further, certain metabolic traits, such as growth on the pentose sugars found in biomass, is not predictive of the ability to ferment these five-carbon sugars to ethanol. Consequently, results from this study show that analyses of relatedness will provide a prediction of which species might provide useful metabolites, but information on the ecology of yeast species is also needed to effectively direct metabolic discovery efforts aimed at improving agricultural utilization and biotechnology.

Technical Abstract: Associations between traits are prevalent in nature, occurring across a diverse range of taxa and traits. The evolution of trait correlations can be driven by factors intrinsic or extrinsic to an organism, but few studies, especially in microbes, have simultaneously investigated both across a broad taxonomic range. Here we quantify pairwise associations among 48 traits across 784 diverse yeast species of the ancient budding yeast subphylum Saccharomycotina, assessing the effects of phylogenetic history, genetics, and ecology. We find extensive pairwise negative and positive pairwise associations among traits and between traits and environments. In particular, positive correlations among carbon utilization traits track with chemical structures and metabolic pathways, while fermentation is negatively correlated with the utilization of the pentose sugars, which are major components of plant biomass. We further describe a suite of traits in mammalian pathogenic and commensal yeasts that includes growth at high temperature and a narrowed panel of carbon sources. These results demonstrate how both intrinsic and extrinsic factors drive the suites of traits present in organisms to evolve convergent physiologies and ecologies in diverse clades across macroevolutionary timescales.