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Title: Variation and selection on codon usage bias across an entire subphylum

Abstract

Variation in synonymous codon usage is abundant across multiple levels of organization: between codons of an amino acid, between genes in a genome, and between genomes of different species. It is now well understood that variation in synonymous codon usage is influenced by mutational bias coupled with both natural selection for translational efficiency and genetic drift, but how these processes shape patterns of codon usage bias across entire lineages remains unexplored. To address this question, we used a rich genomic data set of 327 species that covers nearly one third of the known biodiversity of the budding yeast subphylum Saccharomycotina. We found that, while genome-wide relative synonymous codon usage (RSCU) for all codons was highly correlated with the GC content of the third codon position (GC3), the usage of codons for the amino acids proline, arginine, and glycine was inconsistent with the neutral expectation where mutational bias coupled with genetic drift drive codon usage. Examination between genes’ effective numbers of codons and their GC3 contents in individual genomes revealed that nearly a quarter of genes (381,174/1,683,203; 23%), as well as most genomes (308/327; 94%), significantly deviate from the neutral expectation. Finally, by evaluating the imprint of translational selection on codonmore » usage, measured as the degree to which genes’ adaptiveness to the tRNA pool were correlated with selective pressure, we show that translational selection is widespread in budding yeast genomes (264/327; 81%). These results suggest that the contribution of translational selection and drift to patterns of synonymous codon usage across budding yeasts varies across codons, genes, and genomes; whereas drift is the primary driver of global codon usage across the subphylum, the codon bias of large numbers of genes in the majority of genomes is influenced by translational selection.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1];  [3]
  1. Vanderbilt Univ., Nashville, TN (United States)
  2. Univ. of Wisconsin, Madison, WI (United States)
  3. Stanford Univ., CA (United States). School of Medicine
Publication Date:
Research Org.:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Contributing Org.:
Vanderbilt Univ., Nashville, TN (United States). Advanced Computing Center for Research and Education
OSTI Identifier:
1579355
Grant/Contract Number:  
SC0018409
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Genetics
Additional Journal Information:
Journal Volume: 15; Journal Issue: 7; Journal ID: ISSN 1553-7404
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

LaBella, Abigail L., Opulente, Dana A., Steenwyk, Jacob L., Hittinger, Chris Todd, Rokas, Antonis, and Barsh, Gregory S. Variation and selection on codon usage bias across an entire subphylum. United States: N. p., 2019. Web. doi:10.1371/journal.pgen.1008304.
LaBella, Abigail L., Opulente, Dana A., Steenwyk, Jacob L., Hittinger, Chris Todd, Rokas, Antonis, & Barsh, Gregory S. Variation and selection on codon usage bias across an entire subphylum. United States. doi:10.1371/journal.pgen.1008304.
LaBella, Abigail L., Opulente, Dana A., Steenwyk, Jacob L., Hittinger, Chris Todd, Rokas, Antonis, and Barsh, Gregory S. Wed . "Variation and selection on codon usage bias across an entire subphylum". United States. doi:10.1371/journal.pgen.1008304. https://www.osti.gov/servlets/purl/1579355.
@article{osti_1579355,
title = {Variation and selection on codon usage bias across an entire subphylum},
author = {LaBella, Abigail L. and Opulente, Dana A. and Steenwyk, Jacob L. and Hittinger, Chris Todd and Rokas, Antonis and Barsh, Gregory S.},
abstractNote = {Variation in synonymous codon usage is abundant across multiple levels of organization: between codons of an amino acid, between genes in a genome, and between genomes of different species. It is now well understood that variation in synonymous codon usage is influenced by mutational bias coupled with both natural selection for translational efficiency and genetic drift, but how these processes shape patterns of codon usage bias across entire lineages remains unexplored. To address this question, we used a rich genomic data set of 327 species that covers nearly one third of the known biodiversity of the budding yeast subphylum Saccharomycotina. We found that, while genome-wide relative synonymous codon usage (RSCU) for all codons was highly correlated with the GC content of the third codon position (GC3), the usage of codons for the amino acids proline, arginine, and glycine was inconsistent with the neutral expectation where mutational bias coupled with genetic drift drive codon usage. Examination between genes’ effective numbers of codons and their GC3 contents in individual genomes revealed that nearly a quarter of genes (381,174/1,683,203; 23%), as well as most genomes (308/327; 94%), significantly deviate from the neutral expectation. Finally, by evaluating the imprint of translational selection on codon usage, measured as the degree to which genes’ adaptiveness to the tRNA pool were correlated with selective pressure, we show that translational selection is widespread in budding yeast genomes (264/327; 81%). These results suggest that the contribution of translational selection and drift to patterns of synonymous codon usage across budding yeasts varies across codons, genes, and genomes; whereas drift is the primary driver of global codon usage across the subphylum, the codon bias of large numbers of genes in the majority of genomes is influenced by translational selection.},
doi = {10.1371/journal.pgen.1008304},
journal = {PLoS Genetics},
number = 7,
volume = 15,
place = {United States},
year = {2019},
month = {7}
}

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