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MBE Advance Access originally published online on December 7, 2007
Molecular Biology and Evolution 2008 25(2):287-300; doi:10.1093/molbev/msm252
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© The Author 2007. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Articles

Diversifying Selection and Concerted Evolution of a Type IV Secretion System in Bartonella

Björn Nystedt*,1, A. Carolin Frank*,1,2, Mikael Thollesson* and Siv G. E. Andersson*

* Department of Molecular Evolution, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden

E-mail: siv.andersson{at}ebc.uu.se.

Accepted for publication November 11, 2007.

We have studied the evolution of a type IV secretion system (T4SS), in Bartonella, which is thought to have changed function from conjugation to erythrocyte adherence following a recent horizontal gene transfer event. The system, called Trw, is unique among T4SSs in that genes encoding both exo- and intracellular components are located within the same duplicated fragment. This provides an opportunity to study the influence of selection on proteins involved in host–pathogen interactions. We sequenced the trw locus from several strains of Bartonella henselae and investigated its evolutionary history by comparisons to other Bartonella species. Several instances of recombination and gene conversion events where detected in the 2- to 5-fold duplicated gene fragments encompassing trwJIH, explaining the homogenization of the anchoring protein TrwI and the divergence of the minor pilus protein TrwJ. A phylogenetic analysis of the 7- to 8-fold duplicated gene coding for the major pilus protein TrwL displayed 2 distinct clades, likely representing a subfunctionalization event. The analyses of the B. henselae strains also identified a recent horizontal transfer event of almost the complete trwL region. We suggest that the switch in function of the T4SS was mediated by the duplication of the genes encoding pilus components and their diversification by combinatorial sequence shuffling within and among genomes. We suggest that the pilus proteins have evolved by diversifying selection to match a divergent set of erythrocyte surface structures, consistent with the trench warfare coevolutionary model.

Key Words: type IV secretion system • Bartonella, duplication • recombination • gene conversion • host–pathogen interaction

1 These authors contributed equally to this work.

2 Present address: Smurfit Institute of Genetics, University of Dublin, Trinity College Dublin, Dublin, Ireland.

Edward Holmes, Associate Editor


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