Mycobacterium leprae diversity and population dynamics in medieval Europe from novel ancient genomes.

Ancient DNA Ancient pathogen genomics Leprosaria Mycobacterium leprae Paleomicrobiology Paleopathology Pathogen diversity Pathogen population dynamics

Journal

BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720

Informations de publication

Date de publication:
05 10 2021
Historique:
received: 28 05 2021
accepted: 07 08 2021
entrez: 6 10 2021
pubmed: 7 10 2021
medline: 2 2 2022
Statut: epublish

Résumé

Hansen'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. Here, 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. Our 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.

Sections du résumé

BACKGROUND
Hansen'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.
RESULTS
Here, 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.
CONCLUSIONS
Our 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.

Identifiants

pubmed: 34610848
doi: 10.1186/s12915-021-01120-2
pii: 10.1186/s12915-021-01120-2
pmc: PMC8493730
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

220

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 200368/Z/15/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 2000368/Z/15/Z
Pays : United Kingdom

Informations de copyright

© 2021. The Author(s).

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Auteurs

Saskia Pfrengle (S)

Institute of Evolutionary Medicine, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland.
Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 19-23, 72070, Tübingen, Germany.

Judith Neukamm (J)

Institute of Evolutionary Medicine, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland.
Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 19-23, 72070, Tübingen, Germany.
Institute for Bioinformatics and Medical Informatics, University of Tübingen, Sand 14, 72076, Tübingen, Germany.

Meriam Guellil (M)

Estonian Biocentre, Institute of Genomics, University of Tartu, Riia 23B, 51010, Tartu, Estonia.

Marcel Keller (M)

Estonian Biocentre, Institute of Genomics, University of Tartu, Riia 23B, 51010, Tartu, Estonia.

Martyna Molak (M)

Centre of New Technologies, University of Warsaw, S. Banacha 2c, 02-097, Warsaw, Poland.

Charlotte Avanzi (C)

Mycobacteria Research Laboratories, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, USA.
Swiss and Tropical Public Health Institute, Basel, Switzerland.

Alena Kushniarevich (A)

Estonian Biocentre, Institute of Genomics, University of Tartu, Riia 23B, 51010, Tartu, Estonia.

Núria Montes (N)

Unitat d'Antropologia Biològica, Departament de Biologia Animal, Biologia Vegetal i Ecologia, Universitat Autònoma de Barcelona, 08193 Bellaterra (Cerdanyola del Vallès), Barcelona, Spain.

Gunnar U Neumann (GU)

Max Planck Institute for the Science of Human History, Kahlaische Str. 10, 07745, Jena, Germany.

Ella Reiter (E)

Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 19-23, 72070, Tübingen, Germany.

Rezeda I Tukhbatova (RI)

Max Planck Institute for the Science of Human History, Kahlaische Str. 10, 07745, Jena, Germany.
Laboratory of Structural Biology, Kazan Federal University, Kazan, Russian Federation, 420008.

Nataliya Y Berezina (NY)

Research Institute and Museum of Anthropology, Moscow State University, 125009, Mokhovaya str. 11, Moscow, Russian Federation.

Alexandra P Buzhilova (AP)

Research Institute and Museum of Anthropology, Moscow State University, 125009, Mokhovaya str. 11, Moscow, Russian Federation.

Dmitry S Korobov (DS)

The Institute of Archaeology of the Russian Academy of Sciences, 117292, Dm. Uljanova str. 19, Moscow, Russian Federation.

Stian Suppersberger Hamre (S)

Department of Archaeology, History, Cultural studies and religion, University of Bergen, 5020, Bergen, Norway.

Vitor M J Matos (VMJ)

Department of Life Sciences, University of Coimbra, Research Centre for Anthropology and Health, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal.

Maria T Ferreira (MT)

Laboratory of Forensic Anthropology, Department of Life Sciences, University of Coimbra, Centre for Functional Ecology, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal.
Área de Antropología Física, Departamento de Biodiversidad y Gestión Ambiental, Universidad de León, Campus de Vegazana, 24071, León, Spain.

Laura González-Garrido (L)

Department of Life Sciences, University of Coimbra, Research Centre for Anthropology and Health, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal.
Área de Antropología Física, Departamento de Biodiversidad y Gestión Ambiental, Universidad de León, Campus de Vegazana, 24071, León, Spain.
Institute of Biomedicine (IBIOMED), Universidad de León, Campus de Vegazana, 24071, León, Spain.

Sofia N Wasterlain (SN)

Department of Life Sciences, University of Coimbra, Research Centre for Anthropology and Health, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal.

Célia Lopes (C)

Department of Life Sciences, University of Coimbra, Research Centre for Anthropology and Health, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal.
Laboratory of Biological Anthropology, Department of Biology; School of Science and Technology, University of Évora, Évora, Portugal.

Ana Luisa Santos (AL)

Department of Life Sciences, University of Coimbra, Research Centre for Anthropology and Health, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal.

Nathalie Antunes-Ferreira (N)

Laboratório de Ciências Forenses e Psicológicas Egas Moniz (LCFPEM), Centro de Investigação Interdisciplinar Egas Moniz (CiiEM), Instituto Universitário Egas Moniz, Egas Moniz CRL, Monte de Caparica, Portugal.
Laboratory of Biological Anthropology and Human Osteology (LABOH), CRIA/FCSH, Universidade NOVA de Lisboa, Lisbon, Portugal.

Vitória Duarte (V)

Department of Life Sciences, University of Coimbra, Research Centre for Anthropology and Health, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal.

Ana Maria Silva (AM)

Department of Life Sciences, University of Coimbra, Research Centre for Anthropology and Health, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal.
Laboratory of Forensic Anthropology, Department of Life Sciences, University of Coimbra, Centre for Functional Ecology, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal.
UNIARQ - University of Lisbon, Lisbon, Portugal.

Linda Melo (L)

Department of Life Sciences, University of Coimbra, Research Centre for Anthropology and Health, Calçada Martim de Freitas, 3000-456, Coimbra, Portugal.

Natasa Sarkic (N)

OSTEO Research, Camino de la Iglesia 1, Barrio de mata, Santiuste De Pedraza, 40171, Segovia, Spain.

Lehti Saag (L)

Estonian Biocentre, Institute of Genomics, University of Tartu, Riia 23B, 51010, Tartu, Estonia.

Kristiina Tambets (K)

Estonian Biocentre, Institute of Genomics, University of Tartu, Riia 23B, 51010, Tartu, Estonia.

Philippe Busso (P)

Global Health Institute, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.

Stewart T Cole (ST)

Global Health Institute, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.
Institut Pasteur, 25-28, rue du Docteur Roux, 75724, Paris Cedex 15, France.

Alexei Avlasovich (A)

Department of Archeology, History of Belarus and Special Historical Disciplines, Mogilev State A. Kuleshov University, Str Kosmonavtov 1, Mogilev, 212022, Republic of Belarus.

Charlotte A Roberts (CA)

Department of Archaeology, Durham University, South Road, Durham, DH1 3 LE, UK.

Alison Sheridan (A)

Department of Scottish History and Archaeology, National Museums Scotland, Chambers Street, Edinburgh, EH1 1JF, UK.

Craig Cessford (C)

Department of Archaeology, University of Cambridge, Downing Street, Cambridge, CB2 3ER, UK.

John Robb (J)

Department of Archaeology, University of Cambridge, Downing Street, Cambridge, CB2 3ER, UK.

Johannes Krause (J)

Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 19-23, 72070, Tübingen, Germany.
Max Planck Institute for the Science of Human History, Kahlaische Str. 10, 07745, Jena, Germany.
Senckenberg Centre for Human Evolution and Paleoenvironments, University of Tübingen, Rümelinstrasse 19-23, 72070, Tübingen, Germany.

Christiana L Scheib (CL)

Estonian Biocentre, Institute of Genomics, University of Tartu, Riia 23B, 51010, Tartu, Estonia. cls83@ut.ee.
St John's College, University of Cambridge, Cambridge, CB2 1TP, UK. cls83@ut.ee.

Sarah A Inskip (SA)

School of Archaeology and Ancient History, University of Leicester, Leicester, LE1 7RH, UK. si159@leicester.ac.uk.

Verena J Schuenemann (VJ)

Institute of Evolutionary Medicine, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland. verena.schuenemann@iem.uzh.ch.
Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 19-23, 72070, Tübingen, Germany. verena.schuenemann@iem.uzh.ch.
Senckenberg Centre for Human Evolution and Paleoenvironments, University of Tübingen, Rümelinstrasse 19-23, 72070, Tübingen, Germany. verena.schuenemann@iem.uzh.ch.

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Classifications MeSH