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MBE Advance Access published online on October 19, 2005
Molecular Biology and Evolution, doi:10.1093/molbev/msj036
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© The Author 2005. 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
Accepted October 10, 2005

Research Article

The "Domino Theory" of Gene Death: Gradual and Mass Gene Extinction Events in Three Lineages of Obligate Symbiotic Bacterial Pathogens

Tal Dagan 1, Ran Blekhman 2, and Dan Graur 3*

1 Institüt für Botanik III, Heinrich-Heine Universität Düsseldorf, Universitätsstrasse 1, 40225 Düsseldorf, Germany
2 Bioinformatics Undergraduate Program, Tel Aviv University, Ramat Aviv 69978, Israel
3 Institüt für Botanik III, Heinrich-Heine Universität Düsseldorf, Universitätsstrasse 1, 40225 Düsseldorf, Germany; Department of Biology and Biochemistry, University of Houston, Houston, TX 77204-5001, USA

* To whom correspondence should be addressed.
Dan Graur, E-mail: dgraur{at}uh.edu


  Abstract

During the adaptation of an organism to a parasitic lifestyle, various gene functions may be rendered superfluous due to the fact that the host may supply these needs. As a consequence, obligate symbiotic bacterial pathogens tend to undergo reductive genomic evolution through gene death (nonfunctionalization or pseudogenization) and deletion. Here, we examine the evolutionary sequence of gene-death events during the process of genome miniaturization in three bacterial species that have experienced extensive genome reduction: Mycobacterium leprae, Shigella flexneri, and Salmonella typhi. We infer that in all three lineages, the distribution of functional categories is similar in pseudogenes and genes, but different from that of absent genes. Based on an analysis of evolutionary distances, we propose a two-step "domino effect" model for reductive genome evolution. The process starts with a gradual gene-by-gene-death sequence of events. Eventually, a crucial gene within a complex pathway or network is rendered non-functional triggering a "mass gene extinction" of the dependent genes. In contrast to published reports according to which genes belonging to certain functional categories are prone to non-functionalization more frequently and earlier than genes belonging to other functional categories, we could discern no characteristic regularity in the temporal order of function loss.


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