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Factors driving metabolic diversity in the budding yeast subphylum.

ABSTRACT: BACKGROUND:Associations between traits are prevalent in nature, occurring across a diverse range of taxa and traits. Individual traits may co-evolve with one other, and these correlations can be driven by factors intrinsic or extrinsic to an organism. However, 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. RESULTS:We find extensive negative (traits that tend to not occur together) and positive (traits that tend to co-occur) pairwise associations among traits, as well as between traits and environments. These associations can largely be explained by the biological properties of the traits, such as overlapping biochemical pathways. The isolation environments of the yeasts explain a minor but significant component of the variance, while phylogeny (the retention of ancestral traits in descendant species) plays an even more limited role. Positive correlations are pervasive among carbon utilization traits and track with chemical structures (e.g., glucosides and sugar alcohols) and metabolic pathways, suggesting a molecular basis for the presence of suites of traits. In several cases, characterized genes from model organisms suggest that enzyme promiscuity and overlapping biochemical pathways are likely mechanisms to explain these macroevolutionary trends. Interestingly, fermentation traits are negatively correlated with the utilization of pentose sugars, which are major components of the plant biomass degraded by fungi and present major bottlenecks to the production of cellulosic biofuels. Finally, we show that mammalian pathogenic and commensal yeasts have a suite of traits that includes growth at high temperature and, surprisingly, the utilization of a narrowed panel of carbon sources. CONCLUSIONS:These results demonstrate how both intrinsic physiological factors and extrinsic ecological factors drive the distribution of traits present in diverse organisms across macroevolutionary timescales.

SUBMITTER: Opulente DA

PROVIDER: S-EPMC5833115 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Factors driving metabolic diversity in the budding yeast subphylum.

Opulente Dana A DA Rollinson Emily J EJ Bernick-Roehr Cleome C Hulfachor Amanda Beth AB Rokas Antonis A Kurtzman Cletus P CP Hittinger Chris Todd CT

BMC biology 20180302 1

<h4>Background</h4>Associations between traits are prevalent in nature, occurring across a diverse range of taxa and traits. Individual traits may co-evolve with one other, and these correlations can be driven by factors intrinsic or extrinsic to an organism. However, 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 subphyl ...[more]

PMID: 29499717

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Project description:IntroductionEukaryotic life depends on the functional elements encoded by both the nuclear genome and organellar genomes, such as those contained within the mitochondria. The content, size, and structure of the mitochondrial genome varies across organisms with potentially large implications for phenotypic variance and resulting evolutionary trajectories. Among yeasts in the subphylum Saccharomycotina, extensive differences have been observed in various species relative to the model yeast Saccharomyces cerevisiae, but mitochondrial genome sampling across many groups has been scarce, even as hundreds of nuclear genomes have become available.MethodsBy extracting mitochondrial assemblies from existing short-read genome sequence datasets, we have greatly expanded both the number of available genomes and the coverage across sparsely sampled clades.ResultsComparison of 353 yeast mitochondrial genomes revealed that, while size and GC content were fairly consistent across species, those in the genera Metschnikowia and Saccharomyces trended larger, while several species in the order Saccharomycetales, which includes S. cerevisiae, exhibited lower GC content. Extreme examples for both size and GC content were scattered throughout the subphylum. All mitochondrial genomes shared a core set of protein-coding genes for Complexes III, IV, and V, but they varied in the presence or absence of mitochondrially-encoded canonical Complex I genes. We traced the loss of Complex I genes to a major event in the ancestor of the orders Saccharomycetales and Saccharomycodales, but we also observed several independent losses in the orders Phaffomycetales, Pichiales, and Dipodascales. In contrast to prior hypotheses based on smaller-scale datasets, comparison of evolutionary rates in protein-coding genes showed no bias towards elevated rates among aerobically fermenting (Crabtree/Warburg-positive) yeasts. Mitochondrial introns were widely distributed, but they were highly enriched in some groups. The majority of mitochondrial introns were poorly conserved within groups, but several were shared within groups, between groups, and even across taxonomic orders, which is consistent with horizontal gene transfer, likely involving homing endonucleases acting as selfish elements.DiscussionAs the number of available fungal nuclear genomes continues to expand, the methods described here to retrieve mitochondrial genome sequences from these datasets will prove invaluable to ensuring that studies of fungal mitochondrial genomes keep pace with their nuclear counterparts.

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Factors driving metabolic diversity in the budding yeast subphylum.

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Factors driving metabolic diversity in the budding yeast subphylum.

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