Journal article
Selection-driven cost-efficiency optimization of transcripts modulates gene evolutionary rate in bacteria
- Abstract:
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Background
Most amino acids are encoded by multiple synonymous codons. However, synonymous codons are not used equally, and this biased codon use varies between different organisms. It has previously been shown that both selection acting to increase codon translational efficiency and selection acting to decrease codon biosynthetic cost contribute to differences in codon bias. However, it is unknown how these two factors interact or how they affect molecular sequence evolution.
Results
Through analysis of 1,320 bacterial genomes we show that bacterial genes are subject to multi-objective selection-driven optimization of codon use. Here, selection acts to simultaneously decrease transcript biosynthetic cost and increase transcript translational efficiency, with highly expressed genes under the greatest selection. This optimization is not simply a consequence of the more translationally efficient codons being less expensive to synthesize. Instead, we show that tRNA gene copy number alters the cost-efficiency trade-off of synonymous codons such that for many species, selection acting on transcript biosynthetic cost and translational efficiency act in opposition. Finally, we show that genes highly optimized to reduce cost and increase efficiency show reduced rates of synonymous and non-synonymous mutation.
Conclusions
This analysis provides a simple mechanistic explanation for variation in evolutionary rate between genes that depends on selection-driven cost-efficiency optimization of the transcript. These findings reveal how optimization of resource allocation to mRNA synthesis is a critical factor that determines both the evolution and composition of genes.
- Publication status:
- Published
- Peer review status:
- Peer reviewed
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- Files:
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(Preview, Version of record, pdf, 7.0MB, Terms of use)
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- Publisher copy:
- 10.1186/s13059-018-1480-7
Authors
- Publisher:
- BioMed Central
- Journal:
- Genome Biology More from this journal
- Volume:
- 19
- Pages:
- 102
- Publication date:
- 2018-07-31
- Acceptance date:
- 2018-06-05
- DOI:
- EISSN:
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1465-6906
- ISSN:
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1474-760X
- Keywords:
- Pubs id:
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pubs:856196
- UUID:
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uuid:06d35b3e-9072-400e-80c1-2bd520f79512
- Local pid:
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pubs:856196
- Source identifiers:
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856196
- Deposit date:
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2018-06-06
- ARK identifier:
Terms of use
- Copyright holder:
- Seward and Kelly
- Copyright date:
- 2018
- Notes:
- © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Licence:
- CC Attribution (CC BY)
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