Emergence and spread of Mycobacterium ulcerans at different geographic scales

ABSTRACTThe classical lineage of Mycobacterium ulcerans is the most prevalent clonal group associated with Buruli ulcer in humans. Its reservoir is strongly associated with the environment. We analyzed together 1,045 isolates collected from 13 countries on two continents to define the evolutionary h...

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Main Authors: Martial Briand, Alexandra Boccarossa, Adrien Rieux, Marie-Agnès Jacques, Line Ganlanon, Christian Johnson, Matthieu Eveillard, Laurent Marsollier, Estelle Marion
Format: Article
Language:English
Published: American Society for Microbiology 2024-04-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.03827-23
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author Martial Briand
Alexandra Boccarossa
Adrien Rieux
Marie-Agnès Jacques
Line Ganlanon
Christian Johnson
Matthieu Eveillard
Laurent Marsollier
Estelle Marion
author_facet Martial Briand
Alexandra Boccarossa
Adrien Rieux
Marie-Agnès Jacques
Line Ganlanon
Christian Johnson
Matthieu Eveillard
Laurent Marsollier
Estelle Marion
author_sort Martial Briand
collection DOAJ
description ABSTRACTThe classical lineage of Mycobacterium ulcerans is the most prevalent clonal group associated with Buruli ulcer in humans. Its reservoir is strongly associated with the environment. We analyzed together 1,045 isolates collected from 13 countries on two continents to define the evolutionary history and population dynamics of this lineage. We confirm that this lineage spread over 7,000 years from Australia to Africa with the emergence of outbreaks in distinct waves in the 18th and 19th centuries. In sharp contrast with its global spread over the last century, transmission chains are now mostly local, with little or no dissemination between endemic areas. This study provides new insights into the phylogeography and population dynamics of M. ulcerans, highlighting the importance of comparative genomic analyses to improve our understanding of pathogen transmission.IMPORTANCEMycobacterium ulcerans is an environmental mycobacterial pathogen that can cause Buruli ulcer, a severe cutaneous infection, mostly spread in Africa and Australia. We conducted a large genomic study of M. ulcerans, combining genomic and evolutionary approaches to decipher its evolutionary history and pattern of spread at different geographic scales. At the scale of villages in an endemic area of Benin, the circulating genotypes have been introduced in recent decades and are not randomly distributed along the river. On a global scale, M. ulcerans has been spreading for much longer, resulting in distinct and compartmentalized endemic foci across Africa and Australia.
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spelling doaj.art-1e85e1b797d4451484f319c8b91aca9d2024-04-02T14:16:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-04-0112410.1128/spectrum.03827-23Emergence and spread of Mycobacterium ulcerans at different geographic scalesMartial Briand0Alexandra Boccarossa1Adrien Rieux2Marie-Agnès Jacques3Line Ganlanon4Christian Johnson5Matthieu Eveillard6Laurent Marsollier7Estelle Marion8Univ Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceUniv Angers, CNRS, ESO, Angers, FranceCIRAD, UMR PVBMT, Saint Pierre, La Réunion, FranceUniv Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceCDTLUB Pobè, Fondation Raoul Follereau, Pobè, BeninCIFRED, University of Abomey-Calavi, Abomey-Calavi, BeninINCIT, Inserm, Univ Angers, CHU Angers, Angers, FranceINCIT, Inserm, Univ Angers, CHU Angers, Angers, FranceINCIT, Inserm, Univ Angers, CHU Angers, Angers, FranceABSTRACTThe classical lineage of Mycobacterium ulcerans is the most prevalent clonal group associated with Buruli ulcer in humans. Its reservoir is strongly associated with the environment. We analyzed together 1,045 isolates collected from 13 countries on two continents to define the evolutionary history and population dynamics of this lineage. We confirm that this lineage spread over 7,000 years from Australia to Africa with the emergence of outbreaks in distinct waves in the 18th and 19th centuries. In sharp contrast with its global spread over the last century, transmission chains are now mostly local, with little or no dissemination between endemic areas. This study provides new insights into the phylogeography and population dynamics of M. ulcerans, highlighting the importance of comparative genomic analyses to improve our understanding of pathogen transmission.IMPORTANCEMycobacterium ulcerans is an environmental mycobacterial pathogen that can cause Buruli ulcer, a severe cutaneous infection, mostly spread in Africa and Australia. We conducted a large genomic study of M. ulcerans, combining genomic and evolutionary approaches to decipher its evolutionary history and pattern of spread at different geographic scales. At the scale of villages in an endemic area of Benin, the circulating genotypes have been introduced in recent decades and are not randomly distributed along the river. On a global scale, M. ulcerans has been spreading for much longer, resulting in distinct and compartmentalized endemic foci across Africa and Australia.https://journals.asm.org/doi/10.1128/spectrum.03827-23Mycobacterium ulceransphylogeographyWGSevolution
spellingShingle Martial Briand
Alexandra Boccarossa
Adrien Rieux
Marie-Agnès Jacques
Line Ganlanon
Christian Johnson
Matthieu Eveillard
Laurent Marsollier
Estelle Marion
Emergence and spread of Mycobacterium ulcerans at different geographic scales
Microbiology Spectrum
Mycobacterium ulcerans
phylogeography
WGS
evolution
title Emergence and spread of Mycobacterium ulcerans at different geographic scales
title_full Emergence and spread of Mycobacterium ulcerans at different geographic scales
title_fullStr Emergence and spread of Mycobacterium ulcerans at different geographic scales
title_full_unstemmed Emergence and spread of Mycobacterium ulcerans at different geographic scales
title_short Emergence and spread of Mycobacterium ulcerans at different geographic scales
title_sort emergence and spread of mycobacterium ulcerans at different geographic scales
topic Mycobacterium ulcerans
phylogeography
WGS
evolution
url https://journals.asm.org/doi/10.1128/spectrum.03827-23
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