MBE Advance Access published online on December 21, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl206
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© 2006 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 |
Gene Cluster Analysis Method Identifies Horizontally Transferred Genes with High Reliability and Indicates that They Provide the Main Mechanism of Operon Gain in Eight Species of 
-Proteobacteria
* Center for Information Biology-DNA Data Bank of Japan, National Institute of Genetics, Research Organization of Information and Systems, Mishima, Shizuoka, 411-8540 Japan
Graduate School of Information and Technology, Hokkaido University, Kita 14, Nishi 9, Kita-ku, Sapporo, 060-0814 Japan
Japan Biological Information Research Center, National Institute of Advanced Industrial Science and Technology, AIST Tokyo Waterfront, 2-42 Aomi, Koto-ku, Tokyo 135-0064, Japan
Corresponding author: Ken Nishikawa, Center for Information Biology-DNA Data Bank of Japan, National Institute of Genetics, Research Organization of Information and Systems, Mishima, Shizuoka, 411-8540 Japan, Tel.: +81-55-981-6859, Fax: +81-55-981-6889, E-mail: knishika{at}genes.nig.ac.jp.
Accepted for publication December 19, 2006.
The formation mechanism of operons remains unresolved: operons may form by rearrangements within a genome or by acquisition of genes from other species, i.e., horizontal gene transfer. One hindrance to its elucidation is the unavailability of a method to accurately identify horizontally gene transfer, although it is generally considered to occur. It is critically important first to select horizontally transferred genes reliably and then to determine the extent to which horizontal gene transfer is involved in operon formation. For this purpose we considered indels in terms of gene clusters instead of individual genes and chose candidates of horizontally transferred genes in eight species of Escherichia, Shigella, and Salmonella based on the minimization of indels. To select a benchmark set of positively horizontally transferred genes against which we can evaluate the candidate set, we devised another procedure using intergenetic alignments. Comparison with the benchmark set demonstrated the absence of a significant number of false positives in the candidate set, showing the high reliability of the method. Analyses of Escherichia coli K-12 operons revealed that, although 
20 operons were probably gained from the last common ancestor of the eight 
–proteobacteria, deletion of intervening genes accounts for the formation of no operons, while horizontal transfer expanded two operons and introduced four entire operons. Based on these observations and reasoning, we suggest that the main mechanism of operon gain is horizontal gene transfer, rather than intra-genomic rearrangements. We propose that genes with related essential functions tend to reside in conserved operons, while genes in nonconserved operons mostly confer slight advantage to the organisms and frequently undergo horizontal transfer and decay. Horizontally transferred genes constitute at least 5.5% of the genes in the eight species and approximately 45% of which originate from other –proteobacteria. Genes involved in viral functions and mobile and extrachromosomal element functions are horizontally transferred more often than expected. This finding indicates frequent mediation of horizontal gene transfer by bacteriophages. On the other hand, not only informational genes (those involved in transcription, translation, and related processes), but also operational genes (those involved in housekeeping) are horizontally transferred less frequently than expected.
Key Words: Horizontal gene transfer • operon • evolution • proteobacteria
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