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Journal articles
TbD1 deletion as a driver of the evolutionary success of modern epidemic Mycobacterium tuberculosis lineages
Daria Bottai
1, *
Wafa Frigui
2
Fadel Sayes
2
Mariagrazia Di Luca
1
Dalila Spadoni
1
Alexandre Pawlik
2
Marina Zoppo
1
Mickael Orgeur
2
Varun Khanna
2
David Hardy
3
Sophie Mangenot
4, 5
Valérie Barbe
4, 5
Claudine Médigue
6
Laurence Ma
7
Christiane Bouchier
7
Arianna Tavanti
1
Gerald Larrouy-Maumus
8
Roland Brosch
2, *
*
Corresponding author
6
LABGeM - Analyse Bio-Informatique pour la Génomique et le Métabolisme
UMR 8030 - Génomique métabolique : DRF/JACOB
Daria Bottai 1
Correspondent author
Wafa Frigui 2
Author
Fadel Sayes 2
Author IdHAL : fsayes ORCID : https://orcid.org/0000-0001-7928-6643
Mariagrazia Di Luca 1
Author
Dalila Spadoni 1
Author
Alexandre Pawlik 2
Author IdHAL : apawlik ORCID : https://orcid.org/0000-0002-5680-576X
Marina Zoppo 1
Author
Mickael Orgeur 2
Author
Varun Khanna 2
Author
David Hardy 3
Author IdHAL : david-hardy ORCID : https://orcid.org/0000-0001-5874-4377
Sophie Mangenot 4, 5
Author
Valérie Barbe 4, 5
Author
Claudine Médigue 6
Author
Laurence Ma 7
Author
Christiane Bouchier 7
Author
Arianna Tavanti 1
Author
Gerald Larrouy-Maumus 8
Author
Roland Brosch 2
Correspondent author
1
University of Pisa - Università di Pisa (Lungarno Pacinotti 43 - 56126 Pisa - Italy)
2
Pathogénomique mycobactérienne intégrée - Integrated Mycobacterial Pathogenomics (25-28, rue du docteur Roux
75724 Paris cedex 15 - France)
- Institut Pasteur [Paris] (25-28, rue du docteur Roux, 75724 Paris cedex 15 - France)
- CNRS - Centre National de la Recherche Scientifique : UMR3525 (France)
3
Neuropathologie expérimentale - Experimental neuropathology (Department of Global Health
28 rue du Docteur Roux
75724 Paris Cedex 15 - France)
- Institut Pasteur [Paris] (25-28, rue du docteur Roux, 75724 Paris cedex 15 - France)
- UPD5 - Université Paris Descartes - Paris 5 (12, rue de l'École de Médecine - 75270 Paris cedex 06 - France)
4
GENOSCOPE - Genoscope - Centre national de séquençage [Evry] (2, rue Gaston Crémieux CP5706 91057 EVRY Cedex - France)
- Université Paris-Saclay (Bâtiment Bréguet, 3 Rue Joliot Curie 2e ét, 91190 Gif-sur-Yvette - France)
- DRF (CEA) - Direction de Recherche Fondamentale (CEA) : DRF/JACOB (Direction de Recherche Fondamentale
Fundamental Research Division
CEA Saclay
91191 Gif-sur-Yvette
- France)
- CEA - Commissariat à l'énergie atomique et aux énergies alternatives (Centre de Saclay Centre de Grenoble Centre de Cadarache etc - France)
5
UEVE - Université d'Évry-Val-d'Essonne (Boulevard François Mitterrand 91025 Evry Cedex - France)
6
LABGeM - Analyse Bio-Informatique pour la Génomique et le Métabolisme (France)
- UMR 8030 - Génomique métabolique : DRF/JACOB (GENOSCOPE, 2 rue Gaston Crémieux 91057 Evry Cedex - France)
- GENOSCOPE - Genoscope - Centre national de séquençage [Evry] : DRF/JACOB (2, rue Gaston Crémieux CP5706 91057 EVRY Cedex - France)
- Université Paris-Saclay (Bâtiment Bréguet, 3 Rue Joliot Curie 2e ét, 91190 Gif-sur-Yvette - France)
- DRF (CEA) - Direction de Recherche Fondamentale (CEA) : DRF/JACOB (Direction de Recherche Fondamentale
Fundamental Research Division
CEA Saclay
91191 Gif-sur-Yvette
- France)
- CEA - Commissariat à l'énergie atomique et aux énergies alternatives (Centre de Saclay Centre de Grenoble Centre de Cadarache etc - France)
- UEVE - Université d'Évry-Val-d'Essonne (Boulevard François Mitterrand 91025 Evry Cedex - France)
- CNRS - Centre National de la Recherche Scientifique : UMR8030 (France)
- GENOSCOPE - Genoscope - Centre national de séquençage [Evry] : DRF/JACOB (2, rue Gaston Crémieux CP5706 91057 EVRY Cedex - France)
7
Génomique (Plate-Forme) - Genomics Platform (Pôle BIOMICS, CITECH
28 rue du Docteur Roux, 75724 Paris Cedex 15 - France)
- Institut Pasteur [Paris] (25-28, rue du docteur Roux, 75724 Paris cedex 15 - France)
8
Imperial College London (South Kensington Campus, London SW7 2AZ - United Kingdom)
Abstract : Mycobacterium tuberculosis (Mtb) strains are classified into different phylogenetic lineages (L), three of which (L2/L3/L4) emerged from a common progenitor after the loss of the MmpS6/MmpL6-encoding Mtb-specific deletion 1 region (TbD1). These TbD1-deleted "modern" lineages are responsible for globally-spread tuberculosis epidemics, whereas TbD1-intact "ancestral" lineages tend to be restricted to specific geographical areas, such as South India and South East Asia (L1) or East Africa (L7). By constructing and characterizing a panel of recombinant TbD1-knock-in and knock-out strains and comparison with clinical isolates, here we show that deletion of TbD1 confers to Mtb a significant increase in resistance to oxidative stress and hypoxia, which correlates with enhanced virulence in selected cellular, guinea pig and C3HeB/FeJ mouse infection models, the latter two mirroring in part the development of hypoxic granulomas in human disease progression. Our results suggest that loss of TbD1 at the origin of the L2/L3/L4 Mtb lineages was a key driver for their global epidemic spread and outstanding evolutionary success.
Document type :
Journal articles
Domain :
Complete list of metadata
https://hal-pasteur.archives-ouvertes.fr/pasteur-02473990
Contributor : Laurence Langlais Connect in order to contact the contributor
Submitted on : Tuesday, February 11, 2020 - 10:11:39 AM
Last modification on : Tuesday, January 18, 2022 - 2:26:07 PM
Long-term archiving on: : Tuesday, May 12, 2020 - 1:55:02 PM
Contributor : Laurence Langlais Connect in order to contact the contributor
Submitted on : Tuesday, February 11, 2020 - 10:11:39 AM
Last modification on : Tuesday, January 18, 2022 - 2:26:07 PM
Long-term archiving on: : Tuesday, May 12, 2020 - 1:55:02 PM
File
s41467-020-14508-5.pdf
Publication funded by an institution
Licence
Distributed under a Creative Commons Attribution 4.0 International License
Identifiers
- HAL Id : pasteur-02473990, version 1
- DOI : 10.1038/s41467-020-14508-5
- PUBMED : 32019932
- PUBMEDCENTRAL : PMC7000671
Collections
PASTEUR | CEA | JACOB | CNRS | CEA-DRF | UNIV-PARIS | ANR | GS-BIOSPHERA | GENOSCOPE | CEA-UPSAY | UNIV-EVRY | GS-LIFE-SCIENCES-HEALTH
Citation
Daria Bottai, Wafa Frigui, Fadel Sayes, Mariagrazia Di Luca, Dalila Spadoni, et al.. TbD1 deletion as a driver of the evolutionary success of modern epidemic Mycobacterium tuberculosis lineages. Nature Communications, Nature Publishing Group, 2020, 11 (1), pp.684. ⟨10.1038/s41467-020-14508-5⟩. ⟨pasteur-02473990⟩
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