David M Wagner1, Jennifer Klunk2, Michaela Harbeck3, Alison Devault4, Nicholas Waglechner5, Jason W Sahl6, Jacob Enk2, Dawn N Birdsell1, Melanie Kuch4, Candice Lumibao7, Debi Poinar4, Talima Pearson1, Mathieu Fourment8, Brian Golding9, Julia M Riehm10, David J D Earn11, Sharon Dewitte12, Jean-Marie Rouillard13, Gisela Grupe14, Ingrid Wiechmann15, James B Bliska16, Paul S Keim6, Holger C Scholz10, Edward C Holmes8, Hendrik Poinar17. 1. Center for Microbial Genetics and Genomics and Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, USA. 2. McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, ON, Canada; Department of Biology, McMaster University, Hamilton, ON, Canada. 3. State Collection for Anthropology and Palaeoanatomy, Munich, Germany. 4. McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, ON, Canada. 5. Michael G DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, ON, Canada. 6. Center for Microbial Genetics and Genomics and Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, USA; Translational Genomics Research Institute, Flagstaff, AZ, USA. 7. McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, ON, Canada; Department of Biology, University of Notre Dame, Notre Dame, IN, USA. 8. Marie Bashir Institute for Infectious Diseases and Biosecurity, University of Sydney, Sydney, NSW, Australia. 9. Department of Biology, McMaster University, Hamilton, ON, Canada. 10. Bundeswehr Institute of Microbiology, Munich, Germany. 11. Michael G DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, ON, Canada; Department of Mathematics and Statistics, McMaster University, Hamilton, ON, Canada. 12. Department of Anthropology, University of South Carolina, Columbia, SC, USA; Department of Biological Sciences, University of South Carolina, Columbia, SC, USA. 13. Department of Chemical Engineering, University of Michigan, Ann Arbor, MI, USA; Mycroarray, Ann Arbor, MI, USA. 14. State Collection for Anthropology and Palaeoanatomy, Munich, Germany; Department Biology I, Biodiversity Research/Anthropology, Ludwig-Maximilian University of Munich, Martinsried, Germany. 15. Department of Veterinary Sciences, Institute of Palaeoanatomy, Domestication Research and the History of Veterinary Medicine, Ludwig-Maximilian University of Munich, Martinsried, Germany. 16. Department of Molecular Genetics and Microbiology and Center for Infectious Diseases, Stony Brook University, Stony Brook, NY, USA. 17. McMaster Ancient DNA Centre, Department of Anthropology, McMaster University, Hamilton, ON, Canada; Department of Biology, McMaster University, Hamilton, ON, Canada; Michael G DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, ON, Canada. Electronic address: poinarh@mcmaster.ca.
Abstract
BACKGROUND: Yersinia pestis has caused at least three human plague pandemics. The second (Black Death, 14-17th centuries) and third (19-20th centuries) have been genetically characterised, but there is only a limited understanding of the first pandemic, the Plague of Justinian (6-8th centuries). To address this gap, we sequenced and analysed draft genomes of Y pestis obtained from two individuals who died in the first pandemic. METHODS: Teeth were removed from two individuals (known as A120 and A76) from the early medieval Aschheim-Bajuwarenring cemetery (Aschheim, Bavaria, Germany). We isolated DNA from the teeth using a modified phenol-chloroform method. We screened DNA extracts for the presence of the Y pestis-specific pla gene on the pPCP1 plasmid using primers and standards from an established assay, enriched the DNA, and then sequenced it. We reconstructed draft genomes of the infectious Y pestis strains, compared them with a database of genomes from 131 Y pestis strains from the second and third pandemics, and constructed a maximum likelihood phylogenetic tree. FINDINGS: Radiocarbon dating of both individuals (A120 to 533 AD [plus or minus 98 years]; A76 to 504 AD [plus or minus 61 years]) places them in the timeframe of the first pandemic. Our phylogeny contains a novel branch (100% bootstrap at all relevant nodes) leading to the two Justinian samples. This branch has no known contemporary representatives, and thus is either extinct or unsampled in wild rodent reservoirs. The Justinian branch is interleaved between two extant groups, 0.ANT1 and 0.ANT2, and is distant from strains associated with the second and third pandemics. INTERPRETATION: We conclude that the Y pestis lineages that caused the Plague of Justinian and the Black Death 800 years later were independent emergences from rodents into human beings. These results show that rodent species worldwide represent important reservoirs for the repeated emergence of diverse lineages of Y pestis into human populations. FUNDING: McMaster University, Northern Arizona University, Social Sciences and Humanities Research Council of Canada, Canada Research Chairs Program, US Department of Homeland Security, US National Institutes of Health, Australian National Health and Medical Research Council.
BACKGROUND:Yersinia pestis has caused at least three human plague pandemics. The second (Black Death, 14-17th centuries) and third (19-20th centuries) have been genetically characterised, but there is only a limited understanding of the first pandemic, the Plague of Justinian (6-8th centuries). To address this gap, we sequenced and analysed draft genomes of Y pestis obtained from two individuals who died in the first pandemic. METHODS: Teeth were removed from two individuals (known as A120 and A76) from the early medieval Aschheim-Bajuwarenring cemetery (Aschheim, Bavaria, Germany). We isolated DNA from the teeth using a modified phenol-chloroform method. We screened DNA extracts for the presence of the Y pestis-specific pla gene on the pPCP1 plasmid using primers and standards from an established assay, enriched the DNA, and then sequenced it. We reconstructed draft genomes of the infectious Y pestis strains, compared them with a database of genomes from 131 Y pestis strains from the second and third pandemics, and constructed a maximum likelihood phylogenetic tree. FINDINGS: Radiocarbon dating of both individuals (A120 to 533 AD [plus or minus 98 years]; A76 to 504 AD [plus or minus 61 years]) places them in the timeframe of the first pandemic. Our phylogeny contains a novel branch (100% bootstrap at all relevant nodes) leading to the two Justinian samples. This branch has no known contemporary representatives, and thus is either extinct or unsampled in wild rodent reservoirs. The Justinian branch is interleaved between two extant groups, 0.ANT1 and 0.ANT2, and is distant from strains associated with the second and third pandemics. INTERPRETATION: We conclude that the Y pestis lineages that caused the Plague of Justinian and the Black Death 800 years later were independent emergences from rodents into human beings. These results show that rodent species worldwide represent important reservoirs for the repeated emergence of diverse lineages of Y pestis into human populations. FUNDING: McMaster University, Northern Arizona University, Social Sciences and Humanities Research Council of Canada, Canada Research Chairs Program, US Department of Homeland Security, US National Institutes of Health, Australian National Health and Medical Research Council.
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