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A High-Coverage Yersinia Pestis Genome from a Sixth- Century Justinianic Plague Victim

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A High-Coverage Yersinia Pestis Genome from a Sixth- Century Justinianic Plague Victim A High-Coverage Yersinia pestis Genome from a Sixth- Century Justinianic Plague Victim The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Feldman, M., M. Harbeck, M. Keller, M. A. Spyrou, A. Rott, B. Trautmann, H. C. Scholz, et al. 2016. “A High-Coverage Yersinia pestis Genome from a Sixth-Century Justinianic Plague Victim.” Molecular Biology and Evolution 33 (11): 2911-2923. doi:10.1093/ molbev/msw170. http://dx.doi.org/10.1093/molbev/msw170. Published Version doi:10.1093/molbev/msw170 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:29408370 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA A High-Coverage Yersinia pestis Genome from a Sixth-Century Justinianic Plague Victim Michal Feldman,*,1,3 Michaela Harbeck*,2 Marcel Keller,1,2 Maria A. Spyrou,1,3 Andreas Rott,2 Bernd Trautmann,2 Holger C. Scholz,4,5 Bernd P€affgen,6 Joris Peters,2,7 Michael McCormick,8 Kirsten Bos,1,3 Alexander Herbig,1,3 and Johannes Krause*,1,3 1Max Planck Institute for the Science of Human History, Jena, Germany 2SNSB, State Collection of Anthropology and Palaeoanatomy, Munich, Germany 3Institute for Archaeological Sciences, Archaeo- and Palaeogenetics, University of Tu¨bingen, Tu¨bingen, Germany 4Bundeswehr Institute of Microbiology, Munich, Germany 5German Center for Infection Research (DZIF), Munich, Germany 6Institute for Pre- and Protohistoric Archaeology and Archaeology of the Roman Provinces, Ludwig-Maximilian University Munich, Germany 7Institute of Palaeoanatomy, Domestication Research and the History of Veterinary Medicine, Ludwig-Maximilian University of Munich, Germany 8Department of History, Harvard University, Initiative for the Science of the Human Past *Corresponding authors: E-mails: [email protected]; [email protected]; [email protected]. Associate editor: Connie Mulligan Abstract The Justinianic Plague, which started in the sixth century and lasted to the mid eighth century, is thought to be the first of three historically documented plague pandemics causing massive casualties. Historical accounts and mo- lecular data suggest the bacterium Yersinia pestis as its etiological agent. Here we present a new high-coverage (17.9- fold) Y. pestis genome obtained from a sixth-century skeleton recovered from a southern German burial site close to Munich. The reconstructed genome enabled the detection of 30 unique substitutions as well as structural differ- ences that have not been previously described. We report indels affecting a lacl family transcription regulator gene as well as nonsynonymous substitutions in the nrdE, fadJ, and pcp genes, that have been suggested as plague virulence determinants or have been shown to be upregulated in different models of plague infection. In addition, we identify 19 false positive substitutions in a previously published lower-coverage Y. pestis genome from another archaeological site of the same time period and geographical region that is otherwise genetically identical to the high-coverage genome sequence reported here, suggesting low-genetic diversity of the plague during the sixth century in rural southern Germany. Article Key words: Yersinia pestis, ancient DNA, justinianic plague, whole genome, reconstruction. Introduction Historical records suggest that the first known outbreak of the Justinianic Plague occurred between 541 and AD 543 in The bacterium Yersinia pestis has been infecting humans for Egypt and spread throughout the eastern Roman Empire and over 5,000 years (Rasmussen et al. 2015)andisthoughtre- its neighbors (Little 2007; Stathakopoulos 2004). sponsible for at least three known historic plague pandemics. Contemporary accounts indicate massive mortality caused The first was the sixth- to AD eighth-century Justinianic by the disease that might have contributed to the weakening pandemic, the second started with the infamous Black and the eventual decline of the eastern Roman Empire (Little Death, claiming the lives of up to 50% of the European pop- 2007; Mitchell 2014). The epidemic itself returned in about 18 ulation during the 14th century (Benedictow 2004), and the waves over a period of 200 years until it disappeared in last plague pandemic began in late 19th century China, seed- Europe and the near East in the middle of the 8th century ing many of the plague foci that exist globally today (Pollitzer for yet unknown reasons (Stathakopoulos 2004). 1954; World Health Organization 2004). At present, plague is Apparent discrepancies in epidemiological patterns be- classified as a reemerging infectious disease in certain endemic tween the modern and the historical pandemics have led regions and remains a public health problem with reservoirs scholars to suggest that etiological agents other than Y. pestis on nearly every major continent (World Health Organization may have been responsible for the early and later medieval 2004). pandemics (Cohn 2008; Duncan and Scott 2005; Scott and ß The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] Open Access Mol. Biol. Evol. 33(11):2911–2923 doi:10.1093/molbev/msw170 Advance Access publication August 30, 2016 2911 Feldman et al. doi:10.1093/molbev/msw170 MBE Duncan 2001; Twigg 1984). Molecular evidence obtained of the data enabled a robust phylogenetic and structural from ancient plague victims, however, has established Y. pestis analysis of the Justinianic Y. pestis strain. Comparison of the as at least one of the causative agents for both historical high-coverage genome to the previously published lower-cov- pandemics (Bos et al. 2011; Haensch et al. 2010; Harbeck erage genome suggests that both represent a single strain. et al. 2013; Schuenemann et al. 2011; Wagner et al. 2014; Our analysis confirms the phylogenetic placement previously Wiechmann and Grupe 2005). Nevertheless, the differences suggested; however, we identify 19 out of 176 chromosomal in epidemiology such as the apparently much faster geo- substitutions previously reported in the lower-coverage ge- graphical spread of the historical pandemics compared with nome as false positives. Fourteen of these false positives were the modern third pandemic (Christakos, et al. 2007; Cohn purported as unique substitutions defining the Justinianic 2008; Kanaroglou and Delmelle 2015; Maddicott 1997)still branch. In addition, our high-quality data permitted the iden- need to be addressed. The geographic reach and mortality tification of novel substitutions and structural polymor- impact of individual waves as well as of the Justinianic pan- phisms that are unique to the Justinianic Y. pestis strain. demic as a whole remain unknown. Environmental and be- havioral factors as well as genetic factors in the host, vector or pathogen have been known to alter the disease dynamics in Results and Discussion modern plague outbreaks (Duplantier et al. 2005; Enscore To identify Justinianic Plague victims that could potentially be et al. 2002; Guiyoule et al. 1997; Keim and Wagner 2009; used for Y. pestis genome reconstructions, teeth extracted from Parmenter et al. 1999; Schmid et al. 2015; Xu et al. 2014). 20 skeletons unearthed from double burials in a sixth-century The characterization of historical Y. pestis strains and a com- Bavarian burial ground in Altenerding, southern Germany were parison to extant strains may well shed light on the role of the screened with a conventional polymerase chain reaction (PCR) evolving bacterial genetic structure in forming these notable assay (Seifert et al. 2013). Two adults (AE1175 female/AE1176 epidemiological differences. Moreover, a robust genomic de- male) in the same double burial (Fig. 1, supplementary table S1, scription from the early stages of the Justinianic pandemic Supplementary Material online) generated amplification prod- affords opportunities to trace and understand the evolution ucts of the expected size using primers specific for Y. pestis.An of one of humanity’s most devastating pathogens over a pe- additional qPCR assay amplifying the Y. pestis specific plasmin- riod of deep time, with insights that may illuminate the evo- ogen activator (pla) gene revealed that only individual AE1175, lutionary trajectories of other like organisms. with 90 copies per ml could be a candidate for subsequent Y. Despite their genetic resemblance Y. pestis and its closest pestis genome capture (supplementary fig. S1, Supplementary relative the enteric soil- and water-borne Yersinia pseudotuber- Material online). culosis differ greatly in pathogenicity and transmission Radiocarbon dating suggests the two individuals died be- (Achtman et al. 1999). Furthermore, the Y. pestis genome is tween 426 and AD 571 cal (95.4% probability at 2 sigma); characterized by structural variation caused by frequent intra- grave goods point to a burial in or after 530–570 (supple genomic rearrangements due to abundant insertion sequences, mentary
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