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MBE Advance Access originally published online on March 6, 2006
Molecular Biology and Evolution 2006 23(6):1129-1135; doi:10.1093/molbev/msj120
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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. The online version of this article has been published under an open access model. Users are entitled to use, reproduce, disseminate, or display the open access version of this article for non-commercial purposes provided that: the original authorship is properly and fully attributed; the Journal and Oxford University Press are attributed as the original place of publication with the correct citation details given; if an article is subsequently reproduced or disseminated not in its entirety but only in part or as a derivative work this must be clearly indicated. For commercial re-use, please contact journals.permissions@oxfordjournals.org.

Research Article

Horizontal Transfer of a Virulence Operon to the Ancestor of Mycobacterium tuberculosis

Vania Rosas-Magallanes*, Patrick Deschavanne{dagger}, Lluis Quintana-Murci{ddagger}, Roland Brosch§, Brigitte Gicquel* and Olivier Neyrolles*,||

* Unit of Mycobacterial Genetics, Institut Pasteur, Paris, France; {dagger} Molecular and Genomics Bioinformatics, Institut National de la Santé et de la Recherche Médicale 726, University Paris 7, Paris, France; {ddagger} Centre National de la Recherche Scientifique Formation de Recherche en Evolution 2849, Institut Pasteur, Paris, France; § Unit of Bacterial Molecular Genetics, Institut Pasteur, Paris, France; and || Centre National de la Recherche Scientifique Unité de Recherche Associée 2172, Institut Pasteur, Paris, France

E-mail: neyrolle{at}pasteur.fr.

The contribution of interspecies horizontal gene transfer (HGT) to the evolution and virulence of Mycobacterium tuberculosis, the agent of tuberculosis in humans, has been barely investigated. Here we have studied the evolutionary history of the M. tuberculosis Rv0986-8 virulence operon recently identified, through functional genomics approaches, as playing an important role in parasitism of host phagocytic cells. We showed that among actinobacteria, this operon is specific to the M. tuberculosis complex and to ancestral Mycobacterium prototuberculosis species. These data, together with phylogenetic reconstruction and other in silico analyses, provided strong evidence that this operon has been aquired horizontally by the ancestor of M. tuberculosis, before the recent evolutionary bottleneck that preceded the clonal-like evolution of the M. tuberculosis complex. Genomic signature profiling further suggested that the transfer was plasmid mediated and that the operon originated from a {gamma}-proteobacterium donor species. Our study points out for the first time the contribution of HGT to the emergence of M. tuberculosis and close relatives as major pathogens. In addition, our data underline the importance of deciphering gene transfer networks in M. tuberculosis in order to better understand the evolutionary mechanisms involved in mycobacterial virulence.

Key Words: horizontal gene transfer • Mycobacterium tuberculosis • tuberculosis • virulence


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