Genomic factors shaping codon usage across the Saccharomycotina subphylum
Year: 2024
Type: article
Abstract: Codon usage bias, or the unequal use of synonymous codons, is observed across genes, genomes, and between species. The biased use of synonymous codons has been implicated in many cellular functions, such as translation dynamics and transcript stability, but can also be shaped by neutral forces. The Saccharomycotina, the fungal subphylum containing the yeasts Saccharomyces cerevisiae and Candida albicans , has been a model system for studying codon usage. We characterized codon usage across 1,154 strains from 1,051 species to gain insight into the biases, molecular mechanisms, evolution, and genomic features contributing to codon usage patterns across the subphylum. We found evidence of a general preference for A/T-ending codons and correlations between codon usage bias, GC content, and tRNA-ome size. Codon usage bias is also distinct between the 12 orders within the subphylum to such a degree that yeasts can be classified into orders with an accuracy greater than 90% using a machine learning algorithm trained on codon usage. We also characterized the degree to which codon usage bias is impacted by translational selection. Interestingly, the degree of translational selection was influenced by a combination of genome features and assembly metrics that included the number of coding sequences, BUSCO count, and genome length. Our analysis also revealed an extreme bias in codon usage in the Saccharomycodales associated with a lack of predicted arginine tRNAs. The order contains 24 species, and 23 are computationally predicted to lack tRNAs that decode CGN codons, leaving only the AGN codons to encode arginine. Analysis of Saccharomycodales gene expression, tRNA sequences, and codon evolution suggests that extreme avoidance of the CGN codons is associated with a decline in arginine tRNA function. Codon usage bias within the Saccharomycotina is generally consistent with previous investigations in fungi, which show a role for both genomic features and GC bias in shaping codon usage. However, we find cases of extreme codon usage preference and avoidance along yeast lineages, suggesting additional forces may be shaping the evolution of specific codons.
Source: G3 Genes Genomes Genetics
Institutions: University of North Carolina at Charlotte, Center for Biologics Evaluation and Research, United States Food and Drug Administration, University of Wisconsin–Madison, State University of New York at Oswego, Great Lakes Bioenergy Research Center, Villanova University, Vanderbilt University, Zhejiang University, South China Agricultural University, Westerdijk Fungal Biodiversity Institute
Language: English
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: gold
Estimated APC paid: $2,790
Funders: National Science Foundation, U.S. Department of Energy, U.S. Department of Agriculture, Burroughs Wellcome Fund, Wisconsin Alumni Research Foundation, Norges Idrettshøgskole, National Institutes of Health, National Institute of Food and Agriculture, Office of Science, University of North Carolina at Charlotte, Office of the Vice Chancellor for Research and Graduate Education, University of Wisconsin-Madison, Great Lakes Bioenergy Research Center, Fundamental Research Funds for the Central Universities, National Institute of Allergy and Infectious Diseases, Division of Graduate Education, Biological and Environmental Research, Natural Science Foundation of Zhejiang Province, Science Fund for Distinguished Young Scholars of Zhejiang Province
Awards: G1593943370, G1648283888, Collaborative Research: RoL: The Evolution of the Genotype-Phenotype Map across Budding Yeasts, G3444752832, GREAT LAKES BIOENERGY RESEARCH CENTER, Collaborative Research: RoL: The Evolution of the Genotype-Phenotype Map across Budding Yeasts, G4192505449, G455569901, G4738635193, G4822304152, G5570967653, G608929229, G7157814893, G7302972916, G7350903426, GREAT LAKES BIOENERGY RESEARCH CENTER, G8985330327, Deciphering the phenotypic and genomic traits that underlie the evolution of pathogenicity differences among Aspergillus fumigatus and its close relatives, 媒介害虫水平转移基因大规模筛查与功能鉴定
OpenAlex ID: W4402035282