A molecular portrait of maternal sepsis from Byzantine Troy

Authors: Alison M Devault, Tatum D Mortimer, Andrew Kitchen, Henrike Kiesewetter, Jacob M Enk, G Brian Golding, John Southon, Melanie Kuch, Ana T Duggan, William Aylward, Shea N Gardner, Jonathan E Allen, Andrew M King, Gerard Wright, Makoto Kuroda, Kengo Kato, Derek EG Briggs, Gino Fornaciari, Edward C Holmes, Hendrik N Poinar, Caitlin S Pepperell.

eLife 2017;6:e20983; doi: http://dx.doi.org/10.7554/eLife.20983

Abstract

Pregnancy complications are poorly represented in the archeological record, despite their importance in contemporary and ancient societies. While excavating a Byzantine cemetery in Troy, we discovered calcified abscesses among a woman’s remains. Scanning electron microscopy of the tissue revealed ‘ghost cells’, resulting from dystrophic calcification, which preserved ancient maternal, fetal and bacterial DNA of a severe infection, likely chorioamnionitis. Gardnerella vaginalis and Staphylococcus saprophyticus dominated the abscesses. Phylogenomic analyses of ancient, historical, and contemporary data showed that G. vaginalis Troy fell within contemporary genetic diversity, whereas S. saprophyticus Troy belongs to a lineage that does not appear to be commonly associated with human disease today. We speculate that the ecology of S. saprophyticus infection may have differed in the ancient world as a result of close contacts between humans and domesticated animals. These results highlight the complex and dynamic interactions with our microbial milieu that underlie severe maternal infections.

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17th Century Variola Virus Reveals the Recent History of Smallpox

anasmallpox1

Dr. Ana Duggan examines a piece of mummified tissue.

The partially mummified remains of a young child have offered a unique insight into the history of a once-feared disease. The remains, recovered from the crypt of the Dominican Church of the Holy Spirit in Vilnius, Lithuania, have been dated to the mid-17th century. Despite no visual sign of disease, the mummy yielded a complete genome for variola (major) virus, indicating the presence of a smallpox infection. This 17th century variola strain was found to be ancestral to all known 20th century strains (dating from approximately the end of WWII to the time of smallpox eradication in the late 1970s) which suggests that smallpox is a much more recent infection in humans than previously presumed. Additionally, a reconstruction of the evolutionary history of variola virus hints that the split between the more virulent variola major and the less virulent variola minor forms may have occurred in response to evolutionary pressure by the advent of vaccination in 1796.
Article Title: 17th Century Variola Virus Reveals the Recent History of Smallpox

Authors: Ana T. Duggan, Maria F. Perdomo, Dario Piombino-Mascali, Stephanie Marciniak, Debi Poinar, Matthew V. Emery,  Jan P. Buchmann, Sebastian Duchêne, Rimantas Jankauskas, Margaret Humphreys, G. Brian Golding, John Southon, Alison Devault, Jean-Marie Rouillard, Jason W. Sahl, Olivier Dutour, Klaus Hedman, Antti Sajantila, Geoffrey L. Smith, Edward C. Holmes, and Hendrik N. Poinar

Curr. Biol., Vol. 26, Dec. 2016, DOI: 10.1016/j.cub.2016.10.061

Abstract

Smallpox holds a unique position in the history of medicine. It was the first disease for which a vaccine was developed and remains the only human disease eradicated by vaccination. Although there have been claims of smallpox in Egypt, India, and China dating back millennia, the timescale of emergence of the causative agent, variola virus (VARV), and how it evolved in the context of increasingly widespread immunization, have proven controversial . In particular, some molecular-clock-based studies have suggested that key events in VARV evolution only occurred during the last two centuries and hence in apparent conflict with anecdotal historical reports, although it is difficult to distinguish smallpox from other pustular rashes by description alone. To address these issues, we captured, sequenced, and reconstructed a draft genome of an ancient strain of VARV, sampled from a Lithuanian child mummy dating between 1643 and 1665 and close to the time of several documented European epidemics. When compared to vaccinia virus, this archival strain contained the same pattern of gene degradation as 20th century VARVs, indicating that such loss of gene function had occurred before ca. 1650. Strikingly, the mummy sequence fell basal to all currently sequenced strains of VARV on phylogenetic trees. Molecular-clock analyses revealed a strong clock-like structure and that the timescale of smallpox evolution is more recent than often supposed, with the diversification of major viral lineages only occurring within the 18th and 19th centuries, concomitant with the development of modern vaccination.

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Crypt of the Dominican Church of the Holy Spirit (Vilnius, Lithuania).

k_c_7578

One of the mummies found within the crypt, not examined in this study.

 

Plasmodium falciparum malaria in 1st–2nd century CE southern Italy

Luigi Pigorini National Museum of Prehistory and Ethnography

Lateral view of P. falciparum positive skull from Velia, Italy. Image credit: Luigi Pigorini National Museum of Prehistory and Ethnography

Malaria is an important disease that has long impacted humans in the past and continues to do so today. During the Roman Empire (1st-3rd century C.E.), the parasite is thought to have caused widespread illness and death. Ancient authors describe fevers that sound, in hindsight, like malaria, but the species responsible couldn’t be identified solely using this evidence. To address this, we selected human skeletal samples from diverse coastal and rural localities in southern Italy to see if it was possible to recover molecular signatures of malaria. Using ancient DNA technology, we were able to retrieve over 50% of the Plasmodium falciparum mitochondrial genome from two adults in different localities. This suggests malaria potentially affected individuals in a range of ecological and cultural environments. Although these results definitively place malaria in a specific time and place, much remains to be explored about the extent of this disease in the past and how it influenced daily life in the Empire.

Article Title: Plasmodium falciparum malaria in 1st–2nd century CE southern Italy

Authors: Stephanie Marciniak , Tracy L. Prowse, D. Ann Herring, Jennifer Klunk, Melanie Kuch, Ana T. Duggan, Luca Bondioli, Edward C. Holmes, Hendrik N. Poinar

Curr. Biol., Vol. 26 (23), Dec. 2016, DOI: 10.1016/j.cub.2016.10.016

Article Summary
The historical record attests to the devastation malaria exacted on ancient civilizations, particularly the Roman Empire. However, evidence for the presence of malaria during the Imperial period in Italy (1st–5th century CE) is based on indirect sources, such as historical, epigraphic, or skeletal evidence. Although these sources are crucial for revealing the context of this disease, they cannot establish the causative species of Plasmodium. Importantly, definitive evidence for the presence of malaria is now possible through the implementation of ancient DNA technology. As malaria is presumed to have been at its zenith during the Imperial period, we selected first or second molars from 58 adults from three cemeteries from this time: Isola Sacra (associated with Portus Romae, 1st–3rd century CE), Velia (1st–2nd century CE), and Vagnari (1st–4th century CE). We performed hybridization capture using baits designed from the mitochondrial (mtDNA) genomes of Plasmodium spp. on a prioritized subset of 11 adults (informed by metagenomic sequencing). The mtDNA sequences generated provided compelling phylogenetic evidence for the presence of P. falciparum in two individuals. This is the first genomic data directly implicating P. falciparum in Imperial period southern Italy in adults.

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Luigi Pigorini National Museum of Prehistory and Ethnography in Rome

Frontal view of the above skull. This skull of an adult male (approx. 20-25 years in age), was recovered from the Velia Necropolis (1st-2nd c. C.E). Image credit: Luigi Pigorini National Museum of Prehistory and Ethnography in Rome

 

 

Estimation of gene insertion/deletion rates with missing data

Authors: Utkarsh J. Dang, Alison M. Devault, Tatum D. Mortimer, Caitlin S. Pepperell, Hendrik N. Poinar, and G. Brian Golding

Genetics: Early Online, DOI: 10.1534/genetics.116.191973

Abstract

Lateral gene transfer is an important mechanism for evolution among bacteria. Here, genome-wide gene insertion and deletion rates are modelled in a maximum likelihood framework with the additional flexibility of modelling potential missing data. The performance of the models is illustrated using simulations and a data set on gene family phyletic patterns from Gardnerella vaginalis that includes an ancient taxon. A novel application involving pseudogenization/genome reduction magnitudes is also illustrated using gene family data from Mycobacterium spp. Finally, an R package called indelmiss is available from the Comprehensive R Archive Network at https://cran.r-project.org/package=indelmiss, with support documentation and examples.

Genetics:Early Online Manuscript

North American Mammoth Diversity and Interbreeding

Columbian mammoth

Columbian mammoth. Image credit: Raul Martin

Here we report the sequencing of 67 new mammoths including non-Woolly specimens representing Columbian (Mammuthus columbi), Jeffersonian (Mammuthus jeffersonii), and pygmy (Mammuthus exilis) mammoths. In disagreement with the paleontological record, our analysis suggests that these mammoth species interbred, and may have resulted in specimens displaying intermediate Woolly-Columbian morphologies.

Article Title: Mammuthus Population Dynamics in Late Pleistocene North America: Divergence, Phylogeography, and Introgression

Authors: Jacob Enk, Alison Devault, Christopher Widga, Jeffrey Saunders, Paul Szpak, John Southon, Jean-Marie Rouillard, Beth Shapiro, G. Brian Golding, Grant Zazula, Duane Froese, Daniel C. Fisher, Ross D. E. MacPhee, and Hendrik Poinar

Front. Ecol. Evol., Vol. 4 (42), Apr 2016, DOI: 10.3389/fevo.2016.00042

Abstract

After evolving in Africa at the close of the Miocene, mammoths (Mammuthus sp.) spread through much of the northern hemisphere, diversifying morphologically as they entered various habitats. Paleontologically, these morphs are conventionally recognized as species. In Pleistocene North America alone, several mammoth species have been recognized, inhabiting environments as different as cold tundra-steppe in the north and the arid grasslands or temperate savanna-parklands of the south. Yet mammoth phylogeographic studies have overwhelmingly focused on permafrost-preserved remains of only one of these species, Mammuthus primigenius (woolly mammoth). Here we challenge this bias by performing a geographically and taxonomically wide survey of mammoth genetic diversity across North America. Using a targeted enrichment technique, we sequenced 67 complete mitochondrial genomes including non-primigenius specimens representing Mammuthus columbi (Columbian mammoth), Mammuthus jeffersonii (Jeffersonian mammoth), and Mammuthus exilis (pygmy mammoth), including specimens from contexts not generally associated with good DNA preservation. While we uncovered clear phylogeographic structure in mammoth matrilines, their phylogeny as recovered from mitochondrial DNA is not compatible with existing systematic interpretations of their paleontological record. Instead, our results strongly suggest that various nominal mammoth species interbred, perhaps extensively. We hypothesize that at least two distinct stages of interbreeding between conventional paleontological species are likely responsible for this pattern—one between Siberian woolly mammoths and resident American populations that introduced woolly mammoth phenotypes to the continent, and another between ecomorphologically distinct populations of woolly and Columbian mammoths in North America south of the ice.

Frontiers in Ecology and Evolution Article

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Chris Widga: How Many Mammoths?

Woolly Snowstorm Paleofauna

Woolly Mammoth in a Snowstorm. Image credit: Carl Buell

 

 

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