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Genome Biology and Evolution Advance Access published online on May 5, 2009
Genome Biology and Evolution, doi:10.1093/gbe/evp005
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© 2009 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.

Coevolution of DNA uptake sequences and bacterial proteomes

W. A. Findlay1 and R. J. Redfield2,*

1 Institute for Biological Sciences, National Research Council of Canada, Ottawa ON Canada
2 Dept. of Zoology, University of British Columbia, Vancouver BC Canada

* Address for correspondence: Mailing address: Life Sciences Centre (Zoology), University of British Columbia, 2350 Health Sciences Mall, Vancouver, British Columbia, Canada V6T 1Z3. Phone: (604) 822-3744. Fax: (604) 827-4135. E-mail: redfield{at}zoology.ubc.ca


  Abstract

Dramatic examples of repeated sequences occur in the genomes of some naturally competent bacteria, which contain hundreds or thousands of copies of short motifs called DNA uptake signal sequences. Here we analyze the evolutionary interactions between coding-region uptake sequences and the proteomes of Haemophilus influenzae, Actinobacillus pleuropneumoniae and Neisseria meningitidis. In all three genomes, uptake sequence accumulation in coding sequences has approximately doubled the frequencies of those tripeptides specified by each species’ uptake sequence. The presence of uptake sequences in particular reading frames correlated most strongly with use of preferred codons at degenerately coded positions, but density of uptake sequences correlated only poorly with protein functional category. Genes lacking homologs in related genomes also lacked uptake sequences, strengthening the evidence that uptake sequences do not drive lateral gene transfer between distant relatives but instead accumulate after genes have been transferred. Comparison of the uptake sequence-encoded peptides of H. influenzae and N. meningitidis proteins with their homologs from related bacteria without uptake sequences indicated that uptake sequences were also preferentially located in poorly conserved genes and at poorly conserved amino acids. With few exceptions, amino acids at positions encoded by uptake sequences were as well conserved as other amino acids, suggesting that extant uptake sequences impose little or no constraint on coding for protein function. However this state is likely to be achieved at a substantial cost because of the selective deaths required to eliminate maladaptive mutations that improve uptake sequences.

Keywords: competence; transformation, Haemophilus, Neisseria, Pasteurellaceae

Received February 14, 2009; Revised April 7, 2009; Accepted April 7, 2009


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