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MBE Advance Access published online on November 15, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl174
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© The Author 2006. 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 November 6, 2006

Research Article

Dynamics of Reductive Genome Evolution in Mitochondria and Obligate Intracellular Microbes

Amit N. Khachane 1, Kenneth N. Timmis 1, and Vítor A.P. Martins dos Santos 1 *

1 Department of Environmental Microbiology, Helmholtz Center for Infection Research, Braunschweig, Germany

* To whom correspondence should be addressed.
Vítor A.P. Martins dos Santos, E-mail: vds{at}helmholtz-hzi.de


  Abstract

Reductive evolution in mitochondria and obligate intracellular microbes has led to a significant reduction in their genome size and GC content. We show that genome shrinkage during reductive evolution in prokaryotes follows an exponential decay pattern and provide a method to predict the extent of this decay on an evolutionary time-scale. We validated predictions by comparison with estimated extents of genome reduction known to have occurred in mitochondria and Buchnera aphidicola, through comparative genomics and by drawing on available fossil evidence. The model shows how the mitochondrial ancestor would have quickly shed most of its genome, shortly after its incorporation into the proto-eukaryotic cell, and prior to co-divergence subsequent to the split of eukaryotic lineages. It also predicts that the primary rickettsial parasitic event would have occurred between 140 and 240 million years (Myr) ago, an event of relatively recent evolutionary origin considering the fact that Rickettsia and mitochondria evolved from a common Alphaproteobacterial ancestor. This suggests that the symbiotic events of Rickettsia and mitochondria originated at different time points. Moreover, our model results predicts that the ancestor of Wigglesworthia glossinidia brevipalpis, dated around the time of origin of its symbiotic association with the tsetse fly (50 - 100 Myr ago), was likely to have been an endosymbiont itself, thus supporting an earlier proposition that Wigglesworthia, which is currently a maternally inherited primary endosymbiont, evolved from a secondary endosymbiont.

Keywords: GC content; genome size; mitochondria; obligate intracellular microbes; exponential decay.
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