Ancient Mycobacterium leprae genome reveals medieval English red squirrels as animal leprosy host

• Published in: Current biology Vol. 34; no. 10; pp. 2221 - 2230.e8
• Main Authors: Urban, Christian, Blom, Alette A., Avanzi, Charlotte, Walker-Meikle, Kathleen, Warren, Alaine K., White-Iribhogbe, Katie, Turle, Ross, Marter, Phil, Dawson-Hobbis, Heidi, Roffey, Simon, Inskip, Sarah A., Schuenemann, Verena J.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 20.05.2024
• Subjects: ancient DNA; ancient pathogen genomics; animal hosts of diseases; Animals; Archaeology; DNA, Ancient - analysis; England; Genome, Bacterial; History, Medieval; Humans; Leprosy - history; Leprosy - microbiology; medieval leprosy; Mycobacterium leprae; Mycobacterium leprae - genetics; Mycobacterium leprae - isolation & purification; One Health across time; Phylogeny; Sciuridae - microbiology; England; ancient DNA; medieval leprosy; Mycobacterium leprae; animal hosts of diseases; One Health across time; ancient pathogen genomics
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2024.04.006

Leprosy, one of the oldest recorded diseases in human history, remains prevalent in Asia, Africa, and South America, with over 200,000 cases every year.1,2 Although ancient DNA (aDNA) approaches on the major causative agent, Mycobacterium leprae, have elucidated the disease’s evolutionary history,3,4,5 the role of animal hosts and interspecies transmission in the past remains unexplored. Research has uncovered relationships between medieval strains isolated from archaeological human remains and modern animal hosts such as the red squirrel in England.6,7 However, the time frame, distribution, and direction of transmissions remains unknown. Here, we studied 25 human and 12 squirrel samples from two archaeological sites in Winchester, a medieval English city well known for its leprosarium and connections to the fur trade. We reconstructed four medieval M. leprae genomes, including one from a red squirrel, at a 2.2-fold average coverage. Our analysis revealed a phylogenetic placement of all strains on branch 3 as well as a close relationship between the squirrel strain and one newly reconstructed medieval human strain. In particular, the medieval squirrel strain is more closely related to some medieval human strains from Winchester than to modern red squirrel strains from England, indicating a yet-undetected circulation of M. leprae in non-human hosts in the Middle Ages. Our study represents the first One Health approach for M. leprae in archaeology, which is centered around a medieval animal host strain, and highlights the future capability of such approaches to understand the disease’s zoonotic past and current potential. [Display omitted] •Genetic evidence of M. leprae infection in medieval English red squirrels•Ancient M. leprae squirrel strain related to ancient human strains in the same city•Results suggest a yet-undetected circulation of M. leprae in medieval animal hosts•First One Health approach for M. leprae about a medieval animal strain Urban et al. identify medieval English red squirrels as an animal host for Mycobacterium leprae by genetic evidence. Their One Health approach using historical sources, zooarchaeology, osteoarchaeology, and ancient DNA indicates a previously undetected circulation of M. leprae in non-human hosts in the Middle Ages.