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MBE Advance Access published online on March 5, 2003

Molecular Biology and Evolution, doi:10.1093/molbev/msg022
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2003; all rights reserved
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Accepted September 8, 2002
© 2003 Society for Molecular Biology and Evolution

Original Articles

G+C3 Structuring along the Genome: A Common Feature in Prokaryotes

Vincent Daubin 1* Guy Perrière 1

1 Laboratoire de Biométrie et Biologie Évolutive, UMR CNRS no 5558, Université Claude Bernard - Lyon 1, 43, bd. du 11 Novembre 1918, 69622 Villeurbanne Cedex (France)

* To whom correspondence should be addressed. E-mail: daubin{at}biomserv.univ-lyon1.fr.


   Abstract

The heterogeneity of gene nucleotide content in prokaryotic genomes is commonly interpreted as the result of three main phenomena: i) genes undergo different selection pressures both during and after translation (affecting codon and amino acid choice); ii) genes undergo different mutational pressure whether they are on the leading or lagging strand and iii) genes may have different phylogenetic origins as a result of lateral transfers. However, this view neglects the necessity of organizing genetic information on a chromosome that needs to be replicated and folded, which may add constraints to single gene evolution. As a consequence, genes are potentially submitted to different mutation and selection pressures depending on their position in the genome. In this paper, we analyze the structuring of different codon usage measures along completely sequenced bacterial genomes. We show that most of them are highly structured suggesting that genes have different base content depending on their location on the chromosome. A peculiar pattern of genome structure, with a tendency toward an A+T-enrichment near the replication terminus, is found in most bacterial phyla and may reflect common chromosome constraints. Several species may have lost this pattern probably because of genome rearrangements or integration of foreign DNA. We show that in several species, this enrichment is associated to an increase of evolutionary rate and we discuss the evolutionary implications of these results. We argue that structural constraints acting on the circular chromosome are not negligible and that this natural structuring of bacterial genomes may be a cause of overestimation in lateral gene transfer predictions using codon composition indices.

Key Words: complete genome, bacteria, mutation pressure, G+C content, lateral transfer, evolutionary rate


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