This Article OPEN ACCESS ARTICLE Full Text Full Text (PDF) Supplemental Research Data Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Price, M. N. Articles by Alm, E. J. Search for Related Content PubMed PubMed Citation Articles by Price, M. N. Articles by Alm, E. J. Social Bookmarking                   What's this?

Letter

Operon formation is driven by co-regulation and not by horizontal gene transfer

¹ Lawrence Berkeley Laboratory, Berkeley California, 94720 USA ² Howard Hughes Medical Institute and the Department of Bioengineering, University of California, Berkeley, California, 94720 USA

The organization of bacterial genes into operons was originally ascribed to the benefits of co-regulation. More recently, the "selfish operon" model, in which operons are formed by repeated gain and loss of genes, was proposed. Indeed, operons are often subject to horizontal gene transfer (HGT). On the other hand, non-HGT genes are particularly likely to be in operons. To clarify whether HGT is involved in operon formation, we identified recently formed operons in Escherichia coli K12. We show that genes that have homologs in distantly related bacteria but not in close relatives of E. coli—indicating HGT—form new operons at about the same rates as native genes. Furthermore, genes in new operons are no more likely than other genes to have phylogenetic trees that are inconsistent with the species tree. In contrast, essential genes and ubiquitous genes without paralogs—genes believed to undergo HGT rarely—often form new operons. We conclude that HGT is not a cause of operon formation but instead promotes the prevalence of pre-existing operons. To explain operon formation, we propose that new operons reduce the amount of regulatory information required to specify optimal expression patterns and infer that operons should be more likely to evolve than independent promoters when regulation is complex. Consistent with this hypothesis, operons have greater amounts of conserved regulatory sequences than do individually transcribed genes.

[Supplemental material is available online at www.genome.org.]

Article and publication are at http://www.genome.org/cgi/doi/10.1101/gr.3368805. Freely available online through the Genome Research Immediate Open Access option.

CiteULike    Connotea    Del.icio.us    Digg    Reddit    Technorati    What's this?

This article has been cited by other articles:

				R. W. W. Brouwer, O. P. Kuipers, and S. A. F. T. v. Hijum The relative value of operon predictions Brief Bioinform, April 17, 2008; (2008) bbn019v1. [Abstract] [Full Text] [PDF]

				R. Liu and H. Ochman Origins of Flagellar Gene Operons and Secondary Flagellar Systems J. Bacteriol., October 1, 2007; 189(19): 7098 - 7104. [Abstract] [Full Text] [PDF]

				K. Homma, S. Fukuchi, Y. Nakamura, T. Gojobori, and K. Nishikawa 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 {gamma}-Proteobacteria Mol. Biol. Evol., March 1, 2007; 24(3): 805 - 813. [Abstract] [Full Text] [PDF]

				Y. Nakamura, T. Itoh, and W. Martin Rate and Polarity of Gene Fusion and Fission in Oryza sativa and Arabidopsis thaliana Mol. Biol. Evol., January 1, 2007; 24(1): 110 - 121. [Abstract] [Full Text] [PDF]

				A. D. S. Cameron and R. J. Redfield Non-canonical CRP sites control competence regulons in Escherichia coli and many other {gamma}-proteobacteria Nucleic Acids Res., November 6, 2006; 34(20): 6001 - 6014. [Abstract] [Full Text] [PDF]

				V. Spirin, M. S. Gelfand, A. A. Mironov, and L. A. Mirny A metabolic network in the evolutionary context: Multiscale structure and modularity PNAS, June 6, 2006; 103(23): 8774 - 8779. [Abstract] [Full Text] [PDF]

				T. Kosaka, T. Uchiyama, S.-i. Ishii, M. Enoki, H. Imachi, Y. Kamagata, A. Ohashi, H. Harada, H. Ikenaga, and K. Watanabe Reconstruction and Regulation of the Central Catabolic Pathway in the Thermophilic Propionate-Oxidizing Syntroph Pelotomaculum thermopropionicum J. Bacteriol., January 1, 2006; 188(1): 202 - 210. [Abstract] [Full Text] [PDF]