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MBE Advance Access published online on July 7, 2004
Molecular Biology and Evolution, doi:10.1093/molbev/msh202
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved
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Accepted June 2, 2004

Original Articles

Successful Lateral Transfer Requires Codon Usage Compatibility between Foreign Genes and Recipient Genomes

Arturo Medrano-Soto 1*, Gabriel Moreno-Hagelsieb 1, Pablo Vinuesa 2, J. Andrés Christen 3, Julio Collado-Vides 1

1 Program of Computational Genomics, Centro de Investigación sobre Fijación de Nitrógeno (UNAM), Av. Universidad s/n. Col. Lomas de Chamilpa, POB 565-A, Cuernavaca, Morelos 62210, México
2 Program of Molecular and Microbial Ecology, Centro de Investigación sobre Fijación de Nitrógeno (UNAM), Av. Universidad s/n. Col. Lomas de Chamilpa, POB 565-A, Cuernavaca, Morelos 62210, México
3 Department of Probability and Statistics, Centro de Investigación en Matemáticas, Jalisco s/n. Col. Valenciana, POB 402, Guanajuato, Guanajuato 36240

* To whom correspondence should be addressed. E-mail: amedrano{at}cifn.unam.mx.


  Abstract

We present evidence supporting the notion that codon usage (CU) compatibility between foreign genes and recipient genomes is an important prerequisite to assess the selective advantage of imported functions, and therefore to increase the fixation probability of horizontal gene transfer (HGT) events. This contrasts with the current tendency in research to predict recent HGTs in prokaryotes by assuming that acquired genes generally display poor CU. By looking at the CU level (poor, typical or rich) exhibited by putative xenologs still resembling their original CU, we found that most alien genes predominantly present typical CU immediately upon introgression, thereby suggesting that the role of CU amelioration in HGT has been overemphasized. In our strategy, we first scanned a representative set of 103 complete prokaryotic genomes for all pairs of candidate xenologs (exported/imported genes) displaying similar CU. We applied additional filtering criteria, including phylogenetic validations, to enhance the reliability of our predictions. Our approach makes no assumptions about the CU of foreign genes being typical or atypical within the recipient genome, thus providing a novel unbiased framework to study the evolutionary dynamics of HGT.

Keywords: Horizontal gene transfer; codon usage compatibility; comparative genomics; evolution; Bayesian model.
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