Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI, 53706, USA.
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI, 53706, USA.
BMC Biol. 2018 Mar 2;16(1):26. doi: 10.1186/s12915-018-0498-3.
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.
性状之间的关联在自然界中很普遍，存在于广泛的分类群和性状中。单个性状可能与其他性状共同进化，这些相关性可能是由生物体内部或外部因素驱动的。然而，很少有研究，特别是在微生物中，同时在广泛的分类范围内研究这些相关性。在这里，我们量化了古老的芽殖酵母亚门 Saccharomycotina 中的 784 种不同酵母物种中 48 个性状之间的成对关联，评估了系统发育历史、遗传学和生态学的影响。
我们发现性状之间以及性状与环境之间存在广泛的负（倾向于不一起出现的性状）和正（倾向于共同出现的性状）的成对关联。这些关联在很大程度上可以用性状的生物学特性来解释，例如重叠的生化途径。酵母的隔离环境解释了一小部分但显著的方差，而系统发育（祖先性状在后代物种中的保留）则起了更有限的作用。碳利用性状之间普遍存在正相关，与化学结构（例如糖苷和糖醇）和代谢途径相吻合，这表明了性状套件存在的分子基础。在几种情况下，模型生物的特征基因表明酶的多功能性和重叠的生化途径可能是解释这些宏观进化趋势的机制。有趣的是，发酵性状与戊糖的利用呈负相关，戊糖是真菌降解植物生物质的主要成分，也是纤维素生物燃料生产的主要瓶颈。最后，我们表明哺乳动物致病性和共生酵母具有一系列性状，包括在高温下生长，以及令人惊讶的是，利用更窄的碳源面板。
这些结果表明，内在的生理因素和外在的生态因素如何共同驱动不同生物体在宏观进化时间尺度上的性状分布。
