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Genome Biol Evol. 2016 Jan 8;8(2):387-402. doi: 10.1093/gbe/evw001.

Mycobacterial Pan-Genome Analysis Suggests Important Role of Plasmids in the Radiation of Type VII Secretion Systems.

Author information

1
INSERM U1173, UFR Simone Weil, Versailles-Saint-en-Quentin University, Saint-Quentin-en-Yvelines 78180, France.
2
Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, 75724, Paris Cedex 15, France.
3
Institut Pasteur, Genotyping of Pathogens and Public Health, 75724, Paris Cedex 15, France.
4
UMR8079, Ecologie Systématique Evolution, Univ. Paris-Sud, CNRS, Université Paris-Saclay, Orsay 91400, France.
5
INSERM U1173, UFR Simone Weil, Versailles-Saint-en-Quentin University, Saint-Quentin-en-Yvelines 78180, France AP-HP, Hôpital Ambroise Paré, Service De Microbiologie Et Hygiène, Boulogne-Billancourt, France.
6
Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, 75724, Paris Cedex 15, France roland.brosch@pasteur.fr guillaume.sapriel@uvsq.fr.
7
INSERM U1173, UFR Simone Weil, Versailles-Saint-en-Quentin University, Saint-Quentin-en-Yvelines 78180, France UMR 8212, LSCE, Versailles-Saint-Quentin University, Saint-Quentin-en-Yvelines 78180, France Atelier De Bio-Informatique. Institut De Systématique, Evolution, Biodiversité, ISYEB, UMR 7205, CNRS, MNHN, UPMC, EPHE. Muséum National D'histoire Naturelle, Cedex 05, Paris 75231, France roland.brosch@pasteur.fr guillaume.sapriel@uvsq.fr.

Abstract

In mycobacteria, various type VII secretion systems corresponding to different ESX (ESAT-6 secretory) types, are contributing to pathogenicity, iron acquisition, and/or conjugation. In addition to the known chromosomal ESX loci, the existence of plasmid-encoded ESX systems was recently reported. To investigate the potential role of ESX-encoding plasmids on mycobacterial evolution, we analyzed a large representative collection of mycobacterial genomes, including both chromosomal and plasmid-borne sequences. Data obtained for chromosomal ESX loci confirmed the previous five classical ESX types and identified a novel mycobacterial ESX-4-like type, termed ESX-4-bis. Moreover, analysis of the plasmid-encoded ESX loci showed extensive diversification, with at least seven new ESX profiles, identified. Three of them (ESX-P clusters 1-3) were found in multiple plasmids, while four corresponded to singletons. Our phylogenetic and gene-order-analyses revealed two main groups of ESX types: 1) ancestral types, including ESX-4 and ESX-4-like systems from mycobacterial and non-mycobacterial actinobacteria and 2) mycobacteria-specific ESX systems, including ESX-1-2-3-5 systems and the plasmid-encoded ESX types. Synteny analysis revealed that ESX-P systems are part of phylogenetic groups that derived from a common ancestor, which diversified and resulted in the different ESX types through extensive gene rearrangements. A converging body of evidence, derived from composition bias-, phylogenetic-, and synteny analyses points to a scenario in which ESX-encoding plasmids have been a major driving force for acquisition and diversification of type VII systems in mycobacteria, which likely played (and possibly still play) important roles in the adaptation to new environments and hosts during evolution of mycobacterial pathogenesis.

KEYWORDS:

ESX/type VII secretion systems; horizontal gene transfer; mycobacteria; mycobacterial evolution; phylogeny; tuberculosis; virulence

PMID:
26748339
PMCID:
PMC4779608
DOI:
10.1093/gbe/evw001
[Indexed for MEDLINE]
Free PMC Article

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