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Genome-wide mosaicism within Mycobacterium abscessus: evolutionary and epidemiological implications

BACKGROUND: In mycobacteria, conjugation differs from the canonical Hfr model, but is still poorly understood. Here, we quantified this evolutionary processe in a natural mycobacterial population, taking advantage of a large clinical strain collection of the emerging pathogen Mycobacterium abscessus...

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Autores principales: Sapriel, Guillaume, Konjek, Julie, Orgeur, Mickael, Bouri, Laurent, Frézal, Lise, Roux, Anne-Laure, Dumas, Emilie, Brosch, Roland, Bouchier, Christiane, Brisse, Sylvain, Vandenbogaert, Mathias, Thiberge, Jean-Michel, Caro, Valérie, Ngeow, Yun Fong, Tan, Joon Liang, Herrmann, Jean-Louis, Gaillard, Jean-Louis, Heym, Beate, Wirth, Thierry
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4756508/
https://www.ncbi.nlm.nih.gov/pubmed/26884275
http://dx.doi.org/10.1186/s12864-016-2448-1
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author Sapriel, Guillaume
Konjek, Julie
Orgeur, Mickael
Bouri, Laurent
Frézal, Lise
Roux, Anne-Laure
Dumas, Emilie
Brosch, Roland
Bouchier, Christiane
Brisse, Sylvain
Vandenbogaert, Mathias
Thiberge, Jean-Michel
Caro, Valérie
Ngeow, Yun Fong
Tan, Joon Liang
Herrmann, Jean-Louis
Gaillard, Jean-Louis
Heym, Beate
Wirth, Thierry
author_facet Sapriel, Guillaume
Konjek, Julie
Orgeur, Mickael
Bouri, Laurent
Frézal, Lise
Roux, Anne-Laure
Dumas, Emilie
Brosch, Roland
Bouchier, Christiane
Brisse, Sylvain
Vandenbogaert, Mathias
Thiberge, Jean-Michel
Caro, Valérie
Ngeow, Yun Fong
Tan, Joon Liang
Herrmann, Jean-Louis
Gaillard, Jean-Louis
Heym, Beate
Wirth, Thierry
author_sort Sapriel, Guillaume
collection PubMed
description BACKGROUND: In mycobacteria, conjugation differs from the canonical Hfr model, but is still poorly understood. Here, we quantified this evolutionary processe in a natural mycobacterial population, taking advantage of a large clinical strain collection of the emerging pathogen Mycobacterium abscessus (MAB). RESULTS: Multilocus sequence typing confirmed the existence of three M. abscessus subspecies, and unravelled extensive allelic exchange between them. Furthermore, an asymmetrical gene flow occurring between these main lineages was detected, resulting in highly admixed strains. Intriguingly, these mosaic strains were significantly associated with cystic fibrosis patients with lung infections or chronic colonization. Genome sequencing of those hybrid strains confirmed that half of their genomic content was remodelled in large genomic blocks, leading to original tri-modal ‘patchwork’ architecture. One of these hybrid strains acquired a locus conferring inducible macrolide resistance, and a large genomic insertion from a slowly growing pathogenic mycobacteria, suggesting an adaptive gene transfer. This atypical genomic architecture of the highly recombinogenic strains is consistent with the distributive conjugal transfer (DCT) observed in M. smegmatis. Intriguingly, no known DCT function was found in M. abscessus chromosome, however, a p-RAW-like genetic element was detected in one of the highly admixed strains. CONCLUSION: Taken together, our results strongly suggest that MAB evolution is sporadically punctuated by dramatic genome wide remodelling events. These findings might have far reaching epidemiological consequences for emerging mycobacterial pathogens survey in the context of increasing numbers of rapidly growing mycobacteria and M. tuberculosis co-infections. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2448-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-47565082016-02-18 Genome-wide mosaicism within Mycobacterium abscessus: evolutionary and epidemiological implications Sapriel, Guillaume Konjek, Julie Orgeur, Mickael Bouri, Laurent Frézal, Lise Roux, Anne-Laure Dumas, Emilie Brosch, Roland Bouchier, Christiane Brisse, Sylvain Vandenbogaert, Mathias Thiberge, Jean-Michel Caro, Valérie Ngeow, Yun Fong Tan, Joon Liang Herrmann, Jean-Louis Gaillard, Jean-Louis Heym, Beate Wirth, Thierry BMC Genomics Research Article BACKGROUND: In mycobacteria, conjugation differs from the canonical Hfr model, but is still poorly understood. Here, we quantified this evolutionary processe in a natural mycobacterial population, taking advantage of a large clinical strain collection of the emerging pathogen Mycobacterium abscessus (MAB). RESULTS: Multilocus sequence typing confirmed the existence of three M. abscessus subspecies, and unravelled extensive allelic exchange between them. Furthermore, an asymmetrical gene flow occurring between these main lineages was detected, resulting in highly admixed strains. Intriguingly, these mosaic strains were significantly associated with cystic fibrosis patients with lung infections or chronic colonization. Genome sequencing of those hybrid strains confirmed that half of their genomic content was remodelled in large genomic blocks, leading to original tri-modal ‘patchwork’ architecture. One of these hybrid strains acquired a locus conferring inducible macrolide resistance, and a large genomic insertion from a slowly growing pathogenic mycobacteria, suggesting an adaptive gene transfer. This atypical genomic architecture of the highly recombinogenic strains is consistent with the distributive conjugal transfer (DCT) observed in M. smegmatis. Intriguingly, no known DCT function was found in M. abscessus chromosome, however, a p-RAW-like genetic element was detected in one of the highly admixed strains. CONCLUSION: Taken together, our results strongly suggest that MAB evolution is sporadically punctuated by dramatic genome wide remodelling events. These findings might have far reaching epidemiological consequences for emerging mycobacterial pathogens survey in the context of increasing numbers of rapidly growing mycobacteria and M. tuberculosis co-infections. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2448-1) contains supplementary material, which is available to authorized users. BioMed Central 2016-02-17 /pmc/articles/PMC4756508/ /pubmed/26884275 http://dx.doi.org/10.1186/s12864-016-2448-1 Text en © Sapriel et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Sapriel, Guillaume
Konjek, Julie
Orgeur, Mickael
Bouri, Laurent
Frézal, Lise
Roux, Anne-Laure
Dumas, Emilie
Brosch, Roland
Bouchier, Christiane
Brisse, Sylvain
Vandenbogaert, Mathias
Thiberge, Jean-Michel
Caro, Valérie
Ngeow, Yun Fong
Tan, Joon Liang
Herrmann, Jean-Louis
Gaillard, Jean-Louis
Heym, Beate
Wirth, Thierry
Genome-wide mosaicism within Mycobacterium abscessus: evolutionary and epidemiological implications
title Genome-wide mosaicism within Mycobacterium abscessus: evolutionary and epidemiological implications
title_full Genome-wide mosaicism within Mycobacterium abscessus: evolutionary and epidemiological implications
title_fullStr Genome-wide mosaicism within Mycobacterium abscessus: evolutionary and epidemiological implications
title_full_unstemmed Genome-wide mosaicism within Mycobacterium abscessus: evolutionary and epidemiological implications
title_short Genome-wide mosaicism within Mycobacterium abscessus: evolutionary and epidemiological implications
title_sort genome-wide mosaicism within mycobacterium abscessus: evolutionary and epidemiological implications
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4756508/
https://www.ncbi.nlm.nih.gov/pubmed/26884275
http://dx.doi.org/10.1186/s12864-016-2448-1
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