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Ancient Mycobacterium leprae genome reveals medieval English red squirrels as animal leprosy host
Christian Urban1, Alette A Blom2, Charlotte Avanzi3
1Institute of Evolutionary Medicine, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland; Department of Environmental Sciences, University of Basel, Spalenring 145, 4055 Basel, Switzerland; Functional Genomics Center Zurich, ETH Zurich and University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland.
Abstract:
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.
Insights
Ancient DNA analysis of medieval leprosy strains reveals close links between human and squirrel infections in England. This study uncovers previously unknown animal host involvement in the disease
Area of Science:
- Paleogenomics
- Infectious Disease Evolution
- Archaeological Science
Background:
- Leprosy (Hansen's disease) is an ancient infectious disease caused by Mycobacterium leprae, still prevalent globally.
- Ancient DNA (aDNA) studies have explored Mycobacterium leprae evolution, but the role of animal hosts and interspecies transmission historically remains unclear.
- Previous research suggested links between medieval human leprosy strains and modern animal hosts like red squirrels.
Purpose of the Study:
- To investigate the role of animal hosts and interspecies transmission in medieval leprosy using archaeological samples.
- To reconstruct and analyze ancient Mycobacterium leprae genomes from human and squirrel remains.
- To understand the zoonotic potential and evolutionary history of leprosy in a medieval context.
Main Methods:
- Analysis of 25 human and 12 squirrel samples from two medieval archaeological sites in Winchester, England.
- Reconstruction of four medieval Mycobacterium leprae genomes using ancient DNA (aDNA) techniques.
- Phylogenetic analysis of reconstructed genomes to determine evolutionary relationships.
Main Results:
- Four medieval Mycobacterium leprae genomes were successfully reconstructed, including one from a red squirrel.
- All reconstructed strains belonged to phylogenetic branch 3.
- A close genetic relationship was found between the medieval squirrel strain and a medieval human strain from Winchester, with the squirrel strain being more similar to medieval human strains than to modern squirrel strains.
Conclusions:
- The findings indicate previously undetected circulation of Mycobacterium leprae in non-human hosts, specifically squirrels, during the Middle Ages.
- This study pioneers a One Health approach in leprosy archaeology, focusing on a medieval animal host strain.
- The research highlights the potential of aDNA and One Health strategies to unravel the zoonotic history and current transmission dynamics of leprosy.
