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MBE Advance Access published online on August 6, 2008

Molecular Biology and Evolution, doi:10.1093/molbev/msn173
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© The Author 2008. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

Coevolution of Codon Usage and tRNA Genes Leads to Alternative Stable States of Biased Codon Usage

Paul G. Higgs and Wenqi Ran

Department of Physics and Astronomy, McMaster University, Hamilton, Ontario L8S 4M1, Canada

Tel: (905) 525 9140 ext 26870. Fax: (905) 546 1252. email: higgsp{at}mcmaster.ca

Received for publication April 11, 2008. Revision received July 4, 2008. Accepted for publication July 7, 2008.

The typical number of tRNA genes in bacterial genomes is around 50, but this number varies from under 30 to over 120. We argue that tRNA gene copy numbers evolve in response to translational selection. In rapidly multiplying organisms, the time spent in translation is a limiting factor in cell division; hence it pays to duplicate tRNA genes, thereby increasing the concentration of tRNA molecules in the cell and speeding up translation. In slowly multiplying organisms, translation time is not a limiting factor, so the overall translational cost is minimized by reducing the tRNAs to only one copy of each required gene. Translational selection also causes a preference for codons that are most rapidly translated by the current tRNAs; hence codon usage and tRNA gene content will co-evolve to a state where each is adapted to the other. We show that there is often more than one stable co-evolved state. This explains why different combinations of tRNAs and codon bias can exist for different amino acids in the same organism. We analyze a set of 80 complete bacterial genomes and show that the theory predicts many of the trends that are seen in these data.

Key Words: Codon usage • Translational efficiency • tRNA genes • Translational kinetics


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