Genomic sequencing has accelerated the rate at which the underlying genomic mechanisms of well-established ecologically adapted phenotypes are elucidated. For example, a connection was only recently made between environmental distribution of seeds of different sizes, phenotypic variation in the beaks of Darwin’s finches, and changes in the expression of the protein BMP4. Elucidating the precise relationship between genotype, phenotype, and environment, however, is often challenging. By acting on the interface between genotype, phenotype, and environment, natural selection has given rise to numerous ecological adaptations. The immense diversity of life is due, in part, to adaptation to the wide variety of environmental niches available. Species-specific tRNA adaptation index YPD, Phylogenetically independent contrasts stAI, Phylogenetic generalized least squares PIC, Kyoto Encyclopedia of Genes and Genomes KO, The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Ĭompeting interests: The authors have declared that no competing interests exist. Romnes Faculty Fellow, respectively supported by the Pew Charitable Trusts and the Office of the Vice Chancellor for Research and Graduate Education with funding from the Wisconsin Alumni Research Foundation. is a Pew Scholar in the Biomedical Sciences and a H. DEB-1442113 (to A.R.) and DEB-1442148 (to C.T.H.), in part by the DOE Great Lakes Bioenergy Research Center (DOE BER Office of Science DE-SC0018409), USDA National Institute of Food and Agriculture (Hatch Project 1020204 to C.T.H.), and a Guggenheim fellowship (to A.R). All other information and data generated are available in the supplementary files.įunding: This work was supported by the National Science Foundation under Grant Nos. Data associated with each figure can be found in Supplementary Information file 4. Additional sequence analyses generated in this project, including the reference and annotated gene sequences, are stored in the figshare repository associated with this manuscript ( ). The codon optimization values were obtained from the figshare repository from LaBella et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.ĭata Availability: All analyses were done on publicly available and published genome assemblies and annotations (where available). Received: JAccepted: MaPublished: April 19, 2021Ĭopyright: © 2021 LaBella et al. PLoS Biol 19(4):Īcademic Editor: Csaba Pál, Biological Research Centre, HUNGARY This information may be particularly useful for studying fungal dark matter-species that have yet to be cultured in the lab or have only been identified by genomic material.Ĭitation: LaBella AL, Opulente DA, Steenwyk JL, Hittinger CT, Rokas A (2021) Signatures of optimal codon usage in metabolic genes inform budding yeast ecology. This work suggests that codon optimization harbors information about the metabolic ecology of microbial eukaryotes. We further find a correlation between optimization in the GALactose pathway genes and several genes associated with nutrient sensing and metabolism. For example, optimal codon usage of GAL genes is greater than 85% of all genes in the genome of the major human pathogen Candida albicans (CUG-Ser1 clade) and greater than 75% of genes in the genome of the dairy yeast Kluyveromyces lactis (family Saccharomycetaceae). Optimal codon usage in the GAL pathway is also positively correlated with human-associated ecological niches in yeasts of the CUG-Ser1 clade and with dairy-associated ecological niches in the family Saccharomycetaceae. We find that optimal codon usage in the GAL pathway is positively correlated with quantitative growth on galactose, suggesting that GAL codon optimization reflects increased capacity to grow on galactose. To test this hypothesis, we examined the relationship between optimal codon usage in the classic galactose metabolism ( GAL) pathway and known ecological niches for 329 species of budding yeasts, a diverse subphylum of fungi. Bias toward codons that match the tRNA pool is robustly associated with high gene expression in diverse organisms, suggesting that codon optimization could be used in a reverse ecology framework to identify highly expressed, ecologically relevant genes. One rich, heretofore underutilized, source of ecologically relevant genomic information is codon optimality or adaptation. Reverse ecology is the inference of ecological information from patterns of genomic variation.
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