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Evolution of the RpoS Regulon: Origin of RpoS and the Conservation of RpoS-Dependent Regulation in Bacteria

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Abstract

The RpoS sigma factor in proteobacteria regulates genes in stationary phase and in response to stress. Although of conserved function, the RpoS regulon may have different gene composition across species due to high genomic diversity and to known environmental conditions that select for RpoS mutants. In this study, the distribution of RpoS homologs in prokaryotes and the differential dependence of regulon members on RpoS for expression in two γ-proteobacteria (Escherichia coli and Pseudomonas aeruginosa) were examined. Using a maximum-likelihood phylogeny and reciprocal best hits analysis, we show that the RpoS sigma factor is conserved within γ-, β-, and δ-proteobacteria. Annotated RpoS of Borrelia and the enteric RpoS are postulated to have separate evolutionary origins. To determine the conservation of RpoS-dependent gene expression across species, reciprocal best hits analysis was used to identify orthologs of the E. coli RpoS regulon in the RpoS regulon of P. aeruginosa. Of the 186 RpoS-dependent genes of E. coli, 50 proteins have an ortholog within the P. aeruginosa genome. Twelve genes of the 50 orthologs are RpoS-dependent in both species, and at least four genes are regulated by RpoS in other γ-proteobacteria. Despite RpoS conservation in γ-, β-, and δ-proteobacteria, RpoS regulon composition is subject to modification between species. Environmental selection for RpoS mutants likely contributes to the evolutionary divergence and specialization of the RpoS regulon within different bacterial genomes.

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Acknowledgments

This study was supported by research grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) and Canadian Institutes of Health Research (CIHR) to H.E.S. S.C. was supported by an Ontario Graduate Scholarship. We thank R.A. Morton for help with the reciprocal best hits analysis comparing RpoS regulons, R.S. Gupta for help in the indel search, and A. Pasha for help with programming to identify RpoS homologs as reciprocal best hits. We further thank R.A. Morton, R.S. Gupta, and J. Dushoff for informative discussions on phylogeny construction, and T. Dong, C. Joyce, S. Sathiasothy, J. Wasniewski, and R. Yu for comments on the manuscript and technical assistance.

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  1. Department of Biology, McMaster University, Hamilton, L8S 4K1, ON, Canada

    Sarah M. Chiang & Herb E. Schellhorn

  2. McMaster University, Life Sciences Building, Rm. 433, 1280 Main St. West, Hamilton, L8S 4K1, ON, Canada

    Herb E. Schellhorn

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Chiang, S.M., Schellhorn, H.E. Evolution of the RpoS Regulon: Origin of RpoS and the Conservation of RpoS-Dependent Regulation in Bacteria. J Mol Evol 70, 557–571 (2010). https://doi.org/10.1007/s00239-010-9352-0

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