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MBE Advance Access published online on March 6, 2006
Molecular Biology and Evolution, 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
Accepted March 1, 2006

Research Article

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

Vania Rosas-Magallanes 1, Patrick Deschavanne 2, Lluis Quintana-Murci 3, Roland Brosch 4, Brigitte Gicquel 1, and Olivier Neyrolles 5 *

1 Unit of Mycobacterial Genetics, Institut Pasteur, Paris, France
2 Genomics and Molecular Bioinformatics, INSERM 726, University Paris 7, Paris, France
3 Centre National de la Recherche Scientifique (CNRS) FRE 2849, Institut Pasteur, Paris, France
4 Unit of Bacterial Molecular Genetics, Institut Pasteur, Paris, France
5 CNRS URA 2172, Paris, France

* To whom correspondence should be addressed.
Olivier Neyrolles, E-mail: neyrolle{at}pasteur.fr


  Abstract

The contribution of inter-species 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 M. 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 underlines the importance of deciphering gene transfer networks in M. tuberculosis in order to better understand the evolutionary mechanisms involved in mycobacterial virulence.

Keywords: Horizontal gene transfer; Mycobacterium tuberculosis; Tuberculosis; Virulence.
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