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Salmonella enterica genomes from victims of a major sixteenth-century epidemic in Mexico

Nature Ecology & Evolution volume 2, pages 520–528 (2018)Cite this article

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Abstract

Indigenous populations of the Americas experienced high mortality rates during the early contact period as a result of infectious diseases, many of which were introduced by Europeans. Most of the pathogenic agents that caused these outbreaks remain unknown. Through the introduction of a new metagenomic analysis tool called MALT, applied here to search for traces of ancient pathogen DNA, we were able to identify Salmonella enterica in individuals buried in an early contact era epidemic cemetery at Teposcolula-Yucundaa, Oaxaca in southern Mexico. This cemetery is linked, based on historical and archaeological evidence, to the 1545–1550 ce epidemic that affected large parts of Mexico. Locally, this epidemic was known as ‘cocoliztli’, the pathogenic cause of which has been debated for more than a century. Here, we present genome-wide data from ten individuals for Salmonella enterica subsp. enterica serovar Paratyphi C, a bacterial cause of enteric fever. We propose that S. Paratyphi C be considered a strong candidate for the epidemic population decline during the 1545 cocoliztli outbreak at Teposcolula-Yucundaa.

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Fig. 1: Overview of Teposcolula-Yucundaa.
Fig. 2: MALT analysis and pathogen screening of shotgun data.
Fig. 3: Maximum likelihood trees for S. enterica subsp. enterica phylogeny.

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Acknowledgements

This work was supported by the Max Planck Society (J.K.), the European Research Council (ERC) starting grant APGREID (to J.K.), Social Sciences and Humanities Research Council of Canada postdoctoral fellowship grant 756-2011-501 (to K.I.B.) and the Mäxi Foundation (M.G.C.). We thank the Archaeology Council at Mexico’s INAH and the Teposcolula-Yucundaa Archaeological Project for sampling permissions. We are grateful to A. Wissgott, G. Brandt and V. Schuenemann for assistance with laboratory work, A. Günzel for providing graphical support for Fig. 1 and Supplementary Fig. 10, and R. Barquera, J. Hackett and M. Pi for thoughts and discussion on the manuscript. Part of the data storage and analysis was performed on the computational resource bwGRiD Cluster Tübingen funded by the Ministry of Science, Research and the Arts Baden-Württemberg, and the Universities of the State of Baden-Württemberg, Germany, within the framework programme bwHPC. We thank the MALT user community for helpful comments and bug reports.

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Author notes

  1. Michael G. Campana

    Present address: Smithsonian Conservation Biology Institute, Center for Conservation Genomics, Washington DC, USA

  2. Åshild J. Vågene and Alexander Herbig contributed equally to this work.

Authors and Affiliations

  1. Max Planck Institute for the Science of Human History, Jena, Germany

    Åshild J. Vågene, Alexander Herbig, Christina Warinner, Susanna Sabin, Maria A. Spyrou, Aida Andrades Valtueña, Kirsten I. Bos & Johannes Krause

  2. Institute for Archaeological Sciences, University of Tübingen, Tübingen, Germany

    Åshild J. Vågene, Alexander Herbig, Maria A. Spyrou, Kirsten I. Bos & Johannes Krause

  3. Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA

    Michael G. Campana & Noreen Tuross

  4. Institute of Evolutionary Medicine, University of Zurich, Zurich, Switzerland

    Michael G. Campana

  5. National Institute of Anthropology and History (INAH), Mexico, Teposcolula-Yucundaa Archaeological Project, Mexico City, Mexico

    Nelly M. Robles García

  6. Center for Bioinformatics Tübingen (ZBIT), University of Tübingen, Tübingen, Germany

    Daniel Huson

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Contributions

K.I.B., M.G.C., A.H., N.T. and J.K. conceived the investigation. K.I.B., A.H. Å.J.V., M.G.C. and J.K. designed the experiments. N.M.R.G. provided archaeological information and drawings, submitted INAH permits and assisted in the sampling processes. Å.J.V., M.G.C., S.S., M.A.S. and K.I.B. performed the laboratory work. Å.J.V., A.H., K.I.B., C.W. and A.A.V. performed the analyses. D.H. implemented the MALT algorithm. A.H., J.K. and D.H. designed and set up the MALT ancient DNA analysis pipeline. C.W. performed the ethnohistorical analyses. Å.J.V. and K.I.B. wrote the manuscript with contributions from all authors.

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Correspondence to Alexander Herbig.

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Vågene, Å.J., Herbig, A., Campana, M.G. et al. Salmonella enterica genomes from victims of a major sixteenth-century epidemic in Mexico. Nat Ecol Evol 2, 520–528 (2018). https://doi.org/10.1038/s41559-017-0446-6

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