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MBE Advance Access first published online on April 6, 2006
This version published online on April 28, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msk013
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© The Author 2006. 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. The online version of this article has been published under an open access model. Users are entitled to use, reproduce, disseminate, or display the open access version of this article for non-commercial purposes provided that: the original authorship is properly and fully attributed; the Journal and Oxford University Press are attributed as the original place of publication with the correct citation details given; if an article is subsequently reproduced or disseminated not in its entirety but only in part or as a derivative work this must be clearly indicated. For commercial re-use, please contact journals.permissions@oxfordjournals.org.
Accepted March 29, 2006

Research Article

Evolution of Paralogous Genes: Reconstruction of Genome Rearrangements through Comparison of Multiple Genomes within Staphylococcus aureus

Takeshi Tsuru 1, Mikihiko Kawai 2, Yoko Mizutani-Ui 3, Ikuo Uchiyama 4, and Ichizo Kobayashi 5 *

1 Department of Medical Genome Sciences, Graduate School of Frontier Science, University of Tokyo; Graduate Program in Biophysics and Biochemistry, Graduate School of Science, University of Tokyo; Institute of Medical Science, University of Tokyo
2 Institute of Medical Science, University of Tokyo; Division of Pathology, Immunology and Microbiology, Graduate School of Medicine, University of Tokyo
3 Institute of Medical Science, University of Tokyo
4 Research Center for Computational Science, National Institutes of Natural Sciences
5 Department of Medical Genome Sciences, Graduate School of Frontier Science, University of Tokyo; Graduate Program in Biophysics and Biochemistry, Graduate School of Science, University of Tokyo; Institute of Medical Science, University of Tokyo; Division of Pathology, Immunology and Microbiology, Graduate School of Medicine, University of Tokyo

* To whom correspondence should be addressed.
Ichizo Kobayashi, E-mail: ikobaya{at}ims.u-tokyo.ac.jp


  Abstract

Analysis of evolution of paralogous genes in a genome is central to our understanding of genome evolution. Comparison of closely related bacterial genomes, which has provided clues as to how genome sequences evolve under natural conditions, would help in such an analysis. With species Staphylococcus aureus, whole genome sequences have been decoded for 7 strains. We compared their DNA sequences to detect large genome polymorphisms and to deduce mechanisms of genome rearrangements that have formed each of them. We first compared strains N315 and Mu50, which make one of the most closely related strain pairs, at the single nucleotide resolution to catalogue all the middle-sized (more than 10 bp) to large genome polymorphisms such as indels and substitutions. These polymorphisms include two paralogous gene sets, one in a tandem paralogue gene cluster for toxins in a genomic island and the other in a ribosomal RNA operon. We also focused on two other tandem paralogue gene clusters and Type I restriction-modification genes on the genomic islands. Then we reconstructed rearrangement events responsible for these polymorphisms, in the paralogous genes and the others, with reference to the other 5 genomes. For the tandem paralogue gene clusters, we were able to infer sequences for homologous recombination generating the change in the repeat number. These sequences were conserved among the repeated paralogous units likely because of their functional importance. The sequence specificity (S) subunit of Type I restriction-modification systems showed recombination, likely at the homology of a conserved region, between the two variable regions for sequence specificity. We also noticed novel alleles in the ribosomal RNA operons and suggested a role for illegitimate recombination in their formation. These results revealed importance of recombination involving long conserved sequence in the evolution of paralogous genes in the genome.

Keywords: genome comparison; genome rearrangements; deletion; recombination; restriction-modification.
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