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Population Genomics of Mycobacterium leprae Reveals a New Genotype in Madagascar and the Comoros.

ABSTRACT: Human settlement of Madagascar traces back to the beginning of the first millennium with the arrival of Austronesians from Southeast Asia, followed by migrations from Africa and the Middle East. Remains of these different cultural, genetic, and linguistic legacies are still present in Madagascar and other islands of the Indian Ocean. The close relationship between human migration and the introduction and spread of infectious diseases, a well-documented phenomenon, is particularly evident for the causative agent of leprosy, Mycobacterium leprae. In this study, we used whole-genome sequencing (WGS) and molecular dating to characterize the genetic background and retrace the origin of the M. leprae strains circulating in Madagascar (n = 30) and the Comoros (n = 3), two islands where leprosy is still considered a public health problem and monitored as part of a drug resistance surveillance program. Most M. leprae strains (97%) from Madagascar and Comoros belonged to a new genotype as part of branch 1, closely related to single nucleotide polymorphism (SNP) type 1D, named 1D-Malagasy. Other strains belonged to the genotype 1A (3%). We sequenced 39 strains from nine other countries, which, together with previously published genomes, amounted to 242 genomes that were used for molecular dating. Specific SNP markers for the new 1D-Malagasy genotype were used to screen samples from 11 countries and revealed this genotype to be restricted to Madagascar, with the sole exception being a strain from Malawi. The overall analysis thus ruled out a possible introduction of leprosy by the Austronesian settlers and suggests a later origin from East Africa, the Middle East, or South Asia.

SUBMITTER: Avanzi C

PROVIDER: S-EPMC7233131 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Publications

Population Genomics of <i>Mycobacterium leprae</i> Reveals a New Genotype in Madagascar and the Comoros.

Avanzi Charlotte C Lécorché Emmanuel E Rakotomalala Fetra Angelot FA Benjak Andrej A Rapelanoro Rabenja Fahafahantsoa F Ramarozatovo Lala S LS Cauchoix Bertrand B Rakoto-Andrianarivelo Mala M Tió-Coma Maria M Leal-Calvo Thyago T Busso Philippe P Boy-Röttger Stefanie S Chauffour Aurélie A Rasamoelina Tahinamandrato T Andrianarison Aina A Sendrasoa Fandresena F Spencer John S JS Singh Pushpendra P Dashatwar Digambar Ramchandra DR Narang Rahul R Berland Jean-Luc JL Jarlier Vincent V Salgado Claudio G CG Moraes Milton O MO Geluk Annemieke A Randrianantoandro Andriamira A Cambau Emmanuelle E Cole Stewart T ST

Frontiers in microbiology 20200511

Human settlement of Madagascar traces back to the beginning of the first millennium with the arrival of Austronesians from Southeast Asia, followed by migrations from Africa and the Middle East. Remains of these different cultural, genetic, and linguistic legacies are still present in Madagascar and other islands of the Indian Ocean. The close relationship between human migration and the introduction and spread of infectious diseases, a well-documented phenomenon, is particularly evident for the ...[more]

PMID: 32477280

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Project description:BackgroundHansen's disease (leprosy), widespread in medieval Europe, is today mainly prevalent in tropical and subtropical regions with around 200,000 new cases reported annually. Despite its long history and appearance in historical records, its origins and past dissemination patterns are still widely unknown. Applying ancient DNA approaches to its major causative agent, Mycobacterium leprae, can significantly improve our understanding of the disease's complex history. Previous studies have identified a high genetic continuity of the pathogen over the last 1500 years and the existence of at least four M. leprae lineages in some parts of Europe since the Early Medieval period.ResultsHere, we reconstructed 19 ancient M. leprae genomes to further investigate M. leprae's genetic variation in Europe, with a dedicated focus on bacterial genomes from previously unstudied regions (Belarus, Iberia, Russia, Scotland), from multiple sites in a single region (Cambridgeshire, England), and from two Iberian leprosaria. Overall, our data confirm the existence of similar phylogeographic patterns across Europe, including high diversity in leprosaria. Further, we identified a new genotype in Belarus. By doubling the number of complete ancient M. leprae genomes, our results improve our knowledge of the past phylogeography of M. leprae and reveal a particularly high M. leprae diversity in European medieval leprosaria.ConclusionsOur findings allow us to detect similar patterns of strain diversity across Europe with branch 3 as the most common branch and the leprosaria as centers for high diversity. The higher resolution of our phylogeny tree also refined our understanding of the interspecies transfer between red squirrels and humans pointing to a late antique/early medieval transmission. Furthermore, with our new estimates on the past population diversity of M. leprae, we gained first insights into the disease's global history in relation to major historic events such as the Roman expansion or the beginning of the regular transatlantic long distance trade. In summary, our findings highlight how studying ancient M. leprae genomes worldwide improves our understanding of leprosy's global history and can contribute to current models of M. leprae's worldwide dissemination, including interspecies transmissions.

Dataset Information

Population Genomics of Mycobacterium leprae Reveals a New Genotype in Madagascar and the Comoros.

Publications

Population Genomics of <i>Mycobacterium leprae</i> Reveals a New Genotype in Madagascar and the Comoros.

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