Genomic factors shaping codon usage across the Saccharomycotina subphylum

Codon usage bias, or the unequal use of synonymous codons, is observed across genes, genomes, and between species. It has been implicated in many cellular functions, such as translation dynamics and transcript stability, but can also be shaped by neutral forces. We characterized codon usage across 1,154 strains from 1,051 species from the fungal subphylum Saccharomycotina to gain insight into the biases, molecular mechanisms, evolution, and genomic features contributing to codon usage patterns. We found a general preference for A/T-ending codons and correlations between codon usage bias, GC content, and tRNA-ome size. Codon usage bias is distinct between the 12 orders to such a degree that yeasts can be classified with an accuracy >90% using a machine learning algorithm. We also characterized the degree to which codon usage bias is impacted by translational selection. We found it was influenced by a combination of features, including 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 that decode CGN codons, leaving only the AGN codons to encode arginine. Analysis of Saccharomycodales gene expression, tRNA sequences, and codon evolution suggests that avoidance of the CGN codons is associated with a decline in arginine tRNA function. Consistent with previous findings, codon usage bias within the Saccharomycotina is shaped by genomic features and GC bias. 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.

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Publication Details

Journal
G3 Genes Genomes Genetics
Published
2024-08-30
DOI
https://doi.org/10.1093/g3journal/jkae207
Citations
4
Primary Topic
RNA and protein synthesis mechanisms
Type
article
Field-Weighted Citation Impact
0.94

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article

Genomic factors shaping codon usage across the Saccharomycotina subphylum

Marizeth Groenewald, Kaitlin J. Fisher, Dana A. Opulente, Lauren Dineen et al.
4 citations
G3 Genes Genomes Genetics
RNA and protein synthesis mechanisms
0.94
article

Genomic factors shaping codon usage across the Saccharomycotina subphylum

Marizeth Groenewald, Kaitlin J. Fisher, Dana A. Opulente, Lauren Dineen, John F. Wolters, Marie‐Claire Harrison, Antonis Rokas, Chris Todd Hittinger, Abigail L. LaBella, Xing‐Xing Shen, Xiaofan Zhou, Bryan Zavala
article en
4 citations

Abstract

Codon usage bias, or the unequal use of synonymous codons, is observed across genes, genomes, and between species. It has been implicated in many cellular functions, such as translation dynamics and transcript stability, but can also be shaped by neutral forces. We characterized codon usage across 1,154 strains from 1,051 species from the fungal subphylum Saccharomycotina to gain insight into the biases, molecular mechanisms, evolution, and genomic features contributing to codon usage patterns. We found a general preference for A/T-ending codons and correlations between codon usage bias, GC content, and tRNA-ome size. Codon usage bias is distinct between the 12 orders to such a degree that yeasts can be classified with an accuracy >90% using a machine learning algorithm. We also characterized the degree to which codon usage bias is impacted by translational selection. We found it was influenced by a combination of features, including 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 that decode CGN codons, leaving only the AGN codons to encode arginine. Analysis of Saccharomycodales gene expression, tRNA sequences, and codon evolution suggests that avoidance of the CGN codons is associated with a decline in arginine tRNA function. Consistent with previous findings, codon usage bias within the Saccharomycotina is shaped by genomic features and GC bias. 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.

G3 Genes Genomes GeneticsVol. 14(11)
South China Agricultural University (CN), University of North Carolina at Charlotte (US), Center for Biologics Evaluation and Research (US), United States Food and Drug Administration (US), University of Wisconsin–Madison (US), Vanderbilt University (US), Great Lakes Bioenergy Research Center (US), Westerdijk Fungal Biodiversity Institute (NL), Energy Center of Wisconsin (US), Institut de Biologia Evolutiva (ES), State University of New York at Oswego (US), Zhejiang University (CN), Villanova University (US)
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
Life in Land
Openalex Percentile: Top 25%
RNA and protein synthesis mechanisms
0.94
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