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Journal of Bacteriology, October 2004, p. 6575-6585, Vol. 186, No. 19
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.19.6575-6585.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Genome-Wide Molecular Clock and Horizontal Gene Transfer in Bacterial Evolution

Pavel S. Novichkov,¹ Marina V. Omelchenko,^2,3 Mikhail S. Gelfand,^4,5 Andrei A. Mironov,¹ Yuri I. Wolf,³ and Eugene V. Koonin^3*

Department of Bioengineering and Bioinformatics, Moscow State University,¹ Institute for Problems of Information Transmission RAS,⁴ State Scientific Center GosNIIGenetika, Moscow, Russia,⁵ Department of Pathology, F. E. Hebert School of Medicine, Uniformed Services University of the Health Sciences,² National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland³

Received 7 April 2004/ Accepted 28 June 2004

We describe a simple theoretical framework for identifying orthologous sets of genes that deviate from a clock-like model of evolution. The approach used is based on comparing the evolutionary distances within a set of orthologs to a standard intergenomic distance, which was defined as the median of the distribution of the distances between all one-to-one orthologs. Under the clock-like model, the points on a plot of intergenic distances versus intergenomic distances are expected to fit a straight line. A statistical technique to identify significant deviations from the clock-like behavior is described. For several hundred analyzed orthologous sets representing three well-defined bacterial lineages, the -Proteobacteria, the -Proteobacteria, and the Bacillus-Clostridium group, the clock-like null hypothesis could not be rejected for 70% of the sets, whereas the rest showed substantial anomalies. Subsequent detailed phylogenetic analysis of the genes with the strongest deviations indicated that over one-half of these genes probably underwent a distinct form of horizontal gene transfer, xenologous gene displacement, in which a gene is displaced by an ortholog from a different lineage. The remaining deviations from the clock-like model could be explained by lineage-specific acceleration of evolution. The results indicate that although xenologous gene displacement is a major force in bacterial evolution, a significant majority of orthologous gene sets in three major bacterial lineages evolved in accordance with the clock-like model. The approach described here allows rapid detection of deviations from this mode of evolution on the genome scale.

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* Corresponding author. Mailing address: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894. Phone: (301) 435-5913. Fax: (301) 435-7794. E-mail: koonin{at}ncbi.nlm.nih.gov.

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Journal of Bacteriology, October 2004, p. 6575-6585, Vol. 186, No. 19
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.19.6575-6585.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

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