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

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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https://doi.org/10.1038/s41559-017-0446-6
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. © 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
1Max Planck Institute for the Science of Human History, Jena, Germany. 2Institute for Archaeological Sciences, University of Tübingen, Tübingen, Germany.
3Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA. 4Institute of Evolutionary Medicine, University of Zurich, Zurich,
Switzerland. 5National Institute of Anthropology and History (INAH), Mexico, Teposcolula-Yucundaa Archaeological Project, Mexico City, Mexico. 6Center
for Bioinformatics Tübingen (ZBIT), University of Tübingen, Tübingen, Germany. Present address: 7Smithsonian Conservation Biology Institute, Center for
Conservation Genomics, Washington DC, USA. Åshild J. Vågene and Alexander Herbig contributed equally to this work. *e-mail: herbig@shh.mpg.de;
tuross@fas.harvard.edu; bos@shh.mpg.de; krause@shh.mpg.de
Infectious diseases introduced to the New World following
European contact led to successive outbreaks in many regions
of the Americas that continued well into the nineteenth century.
These often caused high mortality and, therefore, contributed a
central, and often underappreciated, influence on the demographic
collapse of many indigenous populations1–4. Population declines
linked to regionally specific epidemics are estimated to have
reached as high as 95%3, and their genetic impact based on recent
population-based studies of ancient and modern human exome and
mitochondrial data attests to their scale5,6. One hypothesis posits
that the increased susceptibility of New World populations to Old
World diseases facilitated European conquest, whereby rapidly dis-
seminating diseases severely weakened indigenous populations2, in
some cases even before European presence in the region2,7. Well-
characterized infections, such as smallpox, measles, mumps and
influenza, are known causes of later contact era outbreaks; however,
the diseases that are responsible for many early contact period New
World epidemics remain unknown and have been the subject of sci-
entific debate for more than a century2–4,7,8.
Morphological changes in skeletal remains9 and ethnohistorical
accounts10 are often explored as sources for understanding popula-
tion health in the past, although both provide only limited resolution
and have generated speculative and, at times, conflicting hypotheses
about the diseases introduced to New World populations2,3,7,11,12.
Most infectious diseases do not leave characteristic markers on
the skeleton due to their short periods of infectivity, the death of
the victim in the acute phase before skeletal changes formed, or a
lack of osteological involvement9. Although historical descriptions
of infectious disease symptoms can be detailed, they are subject
to cultural biases, are affected by translational inaccuracies, lack
a foundation in germ theory and describe historical forms of a con-
dition that may differ from modern manifestations8,11. In addition,
differential diagnosis based on symptoms alone can be unreliable
even in modern contexts, as many infectious diseases have similar
clinical presentations.
Genome-wide studies of ancient pathogens have proven instru-
mental in both identifying and characterizing past human infec-
tious diseases. These studies have largely been restricted to skeletal
collections where individuals display physical changes consistent
with particular infections13–15, a historical context that links a spe-
cific pathogen to a known epidemiological event16 or an organ-
ism that was identified via targeted molecular screening without
prior indication of its presence17. Recent attempts to circumvent
these limitations have concentrated on broad-spectrum molecular
approaches focused on pathogen detection via fluorescence-hybrid-
ization-based microarray technology18, identification via DNA
enrichment of certain microbial regions19 or computational screen-
ing of non-enriched sequence data against human microbiome data
sets20. These approaches offer improvements, but remain biased in
the bacterial taxa used for species-level assignments. As archaeo-
logical material is expected to harbour an abundance of bacteria
that stem from the depositional context, omission of environmental
taxa in species assignments can lead to false-positive identifications.
Additional techniques for authenticating ancient DNA have been
developed21,22, including the identification of characteristic damage
patterns caused by the deamination of cytosines23, methods that
evaluate evenness of coverage of aligned reads across a reference
genome, or length distributions that consider the degree of frag-
mentation, where ancient molecules are expected to be shorter than
those from modern contaminants24.
Salmonella enterica genomes from victims of a
major sixteenth-century epidemic in Mexico
Åshild J. Vågene1,2, Alexander Herbig 1,2*, Michael G. Campana 3,4,7, Nelly M. Robles García5,
Christina Warinner1, Susanna Sabin1, Maria A. Spyrou1,2, Aida Andrades Valtueña1, Daniel Huson6,
Noreen Tuross3*, Kirsten I. Bos1,2* and Johannes Krause 1,2*
Indigenous populations of the Americas experienced high mortality rates during the early contact period as a result of infec-
tious 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.
NATURE ECOLOGY & EVOLUTION | VOL 2 | MARCH 2018 | 520–528 | www.nature.com/natecolevol
520
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