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Title: Factors driving metabolic diversity in the budding yeast subphylum

Abstract

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. 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 suggestmore » 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. These results demonstrate how both intrinsic physiological factors and extrinsic ecological factors drive the distribution of traits present in diverse organisms across macroevolutionary timescales.« less

Authors:
 [1];  [2];  [3];  [3];  [4];  [5];  [1]
  1. Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics. Genome Center of Wisconsin. Wisconsin Energy Inst. J. F. Crow Inst. for the Study of Evolution. DOE Great Lakes Bioenergy Research Center
  2. Applied Biomathematics, Setauket, NY (United States); East Stroudsburg Univ. of Pennsylvania, PA (United States). Dept. of Biological Sciences
  3. Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics. Genome Center of Wisconsin. Wisconsin Energy Inst. J. F. Crow Inst. for the Study of Evolution
  4. Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences
  5. USDA Agricultural Research Service, Peoria, IL (United States). Mycotoxin Prevention and Applied Microbiology Research Unit. National Center for Agricultural Utilization Research
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States); Vanderbilt Univ., Nashville, TN (United States); USDA Agricultural Research Service, Peoria, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); USDA National Inst. of Food and Agriculture (NIFA)
OSTI Identifier:
1459522
Grant/Contract Number:  
SC0018409; FC02-07ER64494; DEB-1442113; DEB-1442148; 1003258
Resource Type:
Accepted Manuscript
Journal Name:
BMC Biology
Additional Journal Information:
Journal Volume: 16; Journal ID: ISSN 1741-7007
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Opulente, Dana A., Rollinson, Emily J., Bernick-Roehr, Cleome, Hulfachor, Amanda Beth, Rokas, Antonis, Kurtzman, Cletus P., and Hittinger, Chris Todd. Factors driving metabolic diversity in the budding yeast subphylum. United States: N. p., 2018. Web. doi:10.1186/s12915-018-0498-3.
Opulente, Dana A., Rollinson, Emily J., Bernick-Roehr, Cleome, Hulfachor, Amanda Beth, Rokas, Antonis, Kurtzman, Cletus P., & Hittinger, Chris Todd. Factors driving metabolic diversity in the budding yeast subphylum. United States. doi:https://doi.org/10.1186/s12915-018-0498-3
Opulente, Dana A., Rollinson, Emily J., Bernick-Roehr, Cleome, Hulfachor, Amanda Beth, Rokas, Antonis, Kurtzman, Cletus P., and Hittinger, Chris Todd. Fri . "Factors driving metabolic diversity in the budding yeast subphylum". United States. doi:https://doi.org/10.1186/s12915-018-0498-3. https://www.osti.gov/servlets/purl/1459522.
@article{osti_1459522,
title = {Factors driving metabolic diversity in the budding yeast subphylum},
author = {Opulente, Dana A. and Rollinson, Emily J. and Bernick-Roehr, Cleome and Hulfachor, Amanda Beth and Rokas, Antonis and Kurtzman, Cletus P. and Hittinger, Chris Todd},
abstractNote = {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. 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. These results demonstrate how both intrinsic physiological factors and extrinsic ecological factors drive the distribution of traits present in diverse organisms across macroevolutionary timescales.},
doi = {10.1186/s12915-018-0498-3},
journal = {BMC Biology},
number = ,
volume = 16,
place = {United States},
year = {2018},
month = {3}
}

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