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MBE Advance Access published online on September 2, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn192
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© 2008 The Authors
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Research Article

Multiple genome comparison within a bacterial species reveals a unit of evolution spanning two adjacent genes in a tandem paralog cluster

Takeshi Tsuru1,2,3 and Ichizo Kobayashi1,2,3

1 Laboratory of Social Genome Sciences, Department of Medical Genome Sciences, Graduate School of Frontier Sciences, University of Tokyo
2 Graduate Program in Biophysics and Biochemistry, Graduate School of Science, University of Tokyo
3 Institute of Medical Science, University of Tokyo

Corresponding author: Ichizo Kobayashi, Department of Medical Genome Sciences, Graduate School of Frontier Science, University of Tokyo at Institute of Medical Science, University of Tokyo, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan; Tel. +81-3-5449-5326; Fax. +81-3-5449-5422; E-mail ikobaya{at}ims.u-tokyo.ac.jp

Received for publication May 5, 2008. Revision received August 21, 2008. Accepted for publication August 26, 2008.

It has been assumed that an open reading frame (ORF) represents a unit of gene evolution as well as a unit of gene expression and function. In the present work, we report a case in which a unit comprising the 3’ region of an ORF linked to a downstream intergenic region that is in turn linked to the 5’ region of a downstream ORF has been conserved, and has served as the unit of gene evolution. The genes are tandem paralogous genes from the bacterium Staphylococcus aureus, for which more than 10 entire genomes have been sequenced. We compared these multiple genome sequences at a locus for the lpl (lipoprotein-like) cluster (encoding lipoprotein homologs presumably related to their host interaction), in the genomic island termed {nu}Sa{alpha}. A highly conserved nucleotide sequence found within every lpl ORF is likely to provide a site for homologous recombination. Comparison of phylogenies of the 5’-variable region and the 3’-variable region within the same ORF revealed significant incongruence. In contrast, pairs of the 3’-variable region of an ORF and the 5’-variable region of the next downstream ORF gave more congruent phylogenies, with distinct groups of conserved pairs. The intergenic region seemed to have co-evolved with the flanking variable regions. Multiple recombination events at the central conserved region appear to have caused various types of rearrangements among strains, shuffling the two variable regions in one ORF, but maintaining a conserved unit comprising the 3’-variable region, intergenic region, and the 5’-variable region spanning adjacent ORFs. This result has strong impact on our understanding of gene evolution because most gene lineages underwent tandem duplication and then diversified. This work also illustrates the use of multiple genome sequences for high-resolution evolutionary analysis within the same species.

Key Words: Staphylococcus aureus • genome evolution • gene duplication • genome rearrangement • genome comparison • MRSA


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