Bacterial Evolution Recorded in Byzantium

The skeleton of a woman who died 800 years ago on the outskirts of the ancient city of Troy in modern Turkey

Photo: Gebhard Bieg

Byzantine skeleton yields 800-year-old genomes from a fatal infection | University of Wisconsin-Madison News.

A 30 year-old woman who died 800 years ago in what was Troy has unwittingly left us a snapshot of evolving bacteria and a serious infection in humans as it was 800 years ago.

The bacteria were recovered from calcified nodules found just below the ribs of a skeleton of the woman who died during pregnancy and who showed skeletal evidence of a hard, agrarian existence which may have made her vulnerable to infection. The recovered genome of two species of bacteria are of such high quality that they can be used to compare changes in one of the bacteria, Staphylococcus saprophyticus, in the intervening 800 years. The other bacteria, Gardnerella vaginalis, showed little change.

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.

DOI: http://dx.doi.org/10.7554/eLife.20983.001

eLife digest
Why and how have some bacteria evolved to cause illness in humans? One way to study bacterial evolution is to search for ancient samples of bacteria and use DNA sequencing technology to investigate how modern bacteria have changed from their ancestors. Understanding the evolution process may help researchers to understand how some bacteria become resistant to the antibiotics designed to kill them.

Complications that occur during pregnancy, including bacterial infections, have long been a major cause of death for women. Now, Devault, Mortimer et al. have been able to sequence the DNA of bacteria found in tissue collected from a woman buried 800 years ago in a cemetery in Troy. Some of the woman’s tissues had been well preserved because they had calcified (probably as the result of infection), which preserved their structure in a mineralized layer. Two mineralized “nodules” in the body appear to be the remains of abscesses. Some of the human DNA in the nodules came from a male, suggesting that the woman was pregnant with a boy and that the abscesses formed in placental tissue.

Sequencing the DNA of the bacteria in the abscess allowed Devault, Mortimer et al. to diagnose the woman’s infection, which was caused by two types of bacteria. One species, called Gardnerella vaginalis, is found in modern pregnancy-related infections. The DNA of the ancient samples was similar to that of modern bacteria. The other bacteria species was an ancient form of Staphylococcus saprophyticus, a type of bacteria that causes urinary tract infections. However, the DNA of the ancient S. saprophyticus bacteria is quite different to that of the bacteria found in modern humans. Instead, their DNA sequence appears more similar to forms of the bacteria that infect currently livestock. As humans lived closely with their livestock at the time the woman lived, her infection may be due to a type of bacteria that passed easily between humans and animals.

Overall, the results suggest that the disease-causing properties of bacteria can arise from a wide range of sources. In addition, Devault, Mortimer et al. have demonstrated that certain types of tissue found in archeological remains are a potential gold mine of information about the evolution of bacteria and other microbes found in the human body.

DOI: http://dx.doi.org/10.7554/eLife.20983.002

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
A molecular portrait of maternal sepsis from Byzantine Troy
eLife 2017 doi: http://dx.doi.org/10.7554/eLife.20983

Published Open Access. Reprinted under the Creative Commons CC0 1.0 Universal (CCO 1.0) public domain dedication.

Results from the osteological analyses of the Late Byzantine burials from Troy fit well to a picture of a rural population... People were struggling with physical strains and infectious diseases and only a few lived beyond the age of 50. Many newborns did not survive infancy and almost all skeletons of children show signs of malnutrition and infection.

Henrike Kiesewetter. Co-author
Quoted in University of Wisconsin-Madison News

From this sample it seems that S. saprophyticus was in transition from a generalised species that could affect cattle as well as humans to the specialised species we have today where a strain of S. saprophyticus is now specific to humans.

This supports the general view that humans acquire many of our common pathogens (of which we seem to have a very large number compared to other species) due to our close association with domestic animals. This finding can be seen as S. saprophyticus being caught in the act of transitioning from cattle to humans. This is of course entirely as the TOE predicts - an environmental change leads to adaptive evolution as new or changed niches are exploited.

The Troy isolate is in this really interesting position between the cow and human-associated staph. It looks like the bug that caused her disease was in a different niche than what we see associated with human infections today.

Caitlin S Pepperell. Co-author
Quoted in University of Wisconsin-Madison News

The general condition of the skeleton of this relatively young (by today's standards) woman is interesting from a historical perspective too. It shows how difficult life had become for ordinary in the latter stages of the Byzantine Empire - the remnant of the once mighty Roman Empire, or at least of the eastern half of it. A poor diet combined with the hard work needed just to survive made the population susceptible to infection and early death. Most people died by the age of 50 and child mortality due to malnutrition was high. Bacteria such as S. saprophyticus would have found it relatively easy to exploit this weak and vulnerable population.

Creationists who managed to read this far might like to note how the TOE offers a full explanation for the differences between this 800 year-old sample of S. saprophyticus and modern strains and how the evidence from history as well as biology reinforce one another. Maybe a creationist could explain this in terms of intelligent (sic) design.

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