MBE Advance Access originally published online on December 21, 2006
Molecular Biology and Evolution 2007 24(3):805-813; 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 Articles |
Gene Cluster Analysis Method Identifies Horizontally Transferred Genes with High Reliability and Indicates that They Provide the Main Mechanism of Operon Gain in 8 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
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, that is, horizontal gene transfer (HGT). One hindrance to its elucidation is the unavailability of a method to accurately identify HGT, although it is generally considered to occur. It is critically important first to select horizontally transferred (HT) genes reliably and then to determine the extent to which HGT is involved in operon formation. For this purpose, we considered indels in terms of gene clusters instead of individual genes and chose candidates of HT genes in 8 species of Escherichia, Shigella, and Salmonella based on the minimization of indels. To select a benchmark set of positively HT 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 8 
-proteobacteria, deletion of intervening genes accounts for the formation of no operons, whereas horizontal transfer expanded 2 operons and introduced 4 entire operons. Based on these observations and reasoning, we suggest that the main mechanism of operon gain is HGT rather than intragenomic rearrangements. We propose that genes with related essential functions tend to reside in conserved operons, whereas genes in nonconserved operons mostly confer slight advantage to the organisms and frequently undergo horizontal transfer and decay. HT genes constitute at least 5.5% of the genes in the 8 species and approximately 45% of which originate from other -proteobacteria. Genes involved in viral functions and mobile and extrachromosomal element functions are HT more often than expected. This finding indicates frequent mediation of HGT 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 HT less frequently than expected.
Key Words: horizontal gene transfer • operon • evolution • proteobacteria
William Martin, Associate Editor
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