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The evolutionary dynamics of tRNA-gene copy number and codon-use in E. coli.

BACKGROUND: The introduction of foreign DNA by Lateral Gene Transfer (LGT) can quickly and drastically alter genome composition. Problems can arise if the genes introduced by LGT use codons that are not suited to the host’s translational machinery. Here we investigate compensatory adaptation of E. c...

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Autores principales: McDonald, Michael J., Chou, Chih-Hung, Swamy, Krishna BS, Huang, Hsien-Da, Leu, Jun-Yi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4539685/
https://www.ncbi.nlm.nih.gov/pubmed/26282127
http://dx.doi.org/10.1186/s12862-015-0441-y
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author McDonald, Michael J.
Chou, Chih-Hung
Swamy, Krishna BS
Huang, Hsien-Da
Leu, Jun-Yi
author_facet McDonald, Michael J.
Chou, Chih-Hung
Swamy, Krishna BS
Huang, Hsien-Da
Leu, Jun-Yi
author_sort McDonald, Michael J.
collection PubMed
description BACKGROUND: The introduction of foreign DNA by Lateral Gene Transfer (LGT) can quickly and drastically alter genome composition. Problems can arise if the genes introduced by LGT use codons that are not suited to the host’s translational machinery. Here we investigate compensatory adaptation of E. coli in response to the introduction of large volumes of codons that are rarely used by the host genome. RESULTS: We analyze genome sequences from the E. coli/Shigella complex, and find that certain tRNA genes are present in multiple copies in two pathogenic Shigella and O157:H7 subgroups of E. coli. Furthermore, we show that the codons that correspond to these multi-copy number tRNA genes are enriched in the high copy number Selfish Genetic Elements (SGE’s) in Shigella and laterally introduced genes in O157:H7. We analyze the duplicate copies and find evidence for the selective retention of tRNA genes introduced by LGT in response to the changed codon content of the genome. CONCLUSION: These data support a model where the relatively rapid influx of LGT genes and SGE’s introduces a large number of genes maladapted to the host’s translational machinery. Under these conditions, it becomes advantageous for the host to retain tRNA genes that are required for the incorporation of amino acids at these codons. Subsequently, the increased number of copies of these specific tRNA genes adjusts the cellular tRNA pool to the demands set by global shifts in codon usage. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0441-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-45396852015-08-19 The evolutionary dynamics of tRNA-gene copy number and codon-use in E. coli. McDonald, Michael J. Chou, Chih-Hung Swamy, Krishna BS Huang, Hsien-Da Leu, Jun-Yi BMC Evol Biol Research Article BACKGROUND: The introduction of foreign DNA by Lateral Gene Transfer (LGT) can quickly and drastically alter genome composition. Problems can arise if the genes introduced by LGT use codons that are not suited to the host’s translational machinery. Here we investigate compensatory adaptation of E. coli in response to the introduction of large volumes of codons that are rarely used by the host genome. RESULTS: We analyze genome sequences from the E. coli/Shigella complex, and find that certain tRNA genes are present in multiple copies in two pathogenic Shigella and O157:H7 subgroups of E. coli. Furthermore, we show that the codons that correspond to these multi-copy number tRNA genes are enriched in the high copy number Selfish Genetic Elements (SGE’s) in Shigella and laterally introduced genes in O157:H7. We analyze the duplicate copies and find evidence for the selective retention of tRNA genes introduced by LGT in response to the changed codon content of the genome. CONCLUSION: These data support a model where the relatively rapid influx of LGT genes and SGE’s introduces a large number of genes maladapted to the host’s translational machinery. Under these conditions, it becomes advantageous for the host to retain tRNA genes that are required for the incorporation of amino acids at these codons. Subsequently, the increased number of copies of these specific tRNA genes adjusts the cellular tRNA pool to the demands set by global shifts in codon usage. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0441-y) contains supplementary material, which is available to authorized users. BioMed Central 2015-08-19 /pmc/articles/PMC4539685/ /pubmed/26282127 http://dx.doi.org/10.1186/s12862-015-0441-y Text en © McDonald et al. 2015 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.
spellingShingle Research Article
McDonald, Michael J.
Chou, Chih-Hung
Swamy, Krishna BS
Huang, Hsien-Da
Leu, Jun-Yi
The evolutionary dynamics of tRNA-gene copy number and codon-use in E. coli.
title The evolutionary dynamics of tRNA-gene copy number and codon-use in E. coli.
title_full The evolutionary dynamics of tRNA-gene copy number and codon-use in E. coli.
title_fullStr The evolutionary dynamics of tRNA-gene copy number and codon-use in E. coli.
title_full_unstemmed The evolutionary dynamics of tRNA-gene copy number and codon-use in E. coli.
title_short The evolutionary dynamics of tRNA-gene copy number and codon-use in E. coli.
title_sort evolutionary dynamics of trna-gene copy number and codon-use in e. coli.
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4539685/
https://www.ncbi.nlm.nih.gov/pubmed/26282127
http://dx.doi.org/10.1186/s12862-015-0441-y
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