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Single Plague Lineage Led to Ancient, Modern Disease Outbreaks

Arnold Böcklin: The Plague (1898)

NEW YORK (GenomeWeb) – A single lineage of the plague has been the cause of both ancient and modern disease outbreaks, according to a new genomic analysis.

A team led by researchers at the Max Planck Institute for the Science of Human History collected DNA samples from plague victims in Spain, Russia, and Germany to fill in the phylogenetic tree of the disease-causing bacterium Yersinia pestis, and to trace its route through Europe and Asia. As they reported today in Cell Host & Microbe, there was likely one introduction of Y. pestis into Europe that then spread to China where it is now the source of modern plague epidemics.

"Our study is the first to provide genetic support for plague's travel from Europe into Asia after the Black Death, and it establishes a link between the Black Death in the mid-14th century and modern plague," first author and Max Planck researcher Maria Spyrou said in a statement.

There have been three human plague pandemics: the Plague of Justinian from the sixth century to eighth century AD; the Black Death in Europe from the 14th century to 18th century; and the Third Pandemic, which emerged in China in the mid-19th century. Y. pestis has been linked to all three outbreaks, but how the plague swept through Europe and Asia hasn't been clear.

Spyrou and her colleagues collected samples from mass graves in Barcelona, Spain, and in Ellwangen, Germany, and from a single grave in Bolgar City, Russia. A combination of artifacts and radiocarbon dating placed the ages of those samples to between 1300 and 1420 AD for the Spanish samples; 1298 and 1388 for the Russian samples; and 1486 and 1627 for the German ones.

The researchers amassed 223 DNA extracts from the teeth of 178 individuals from these graves and gauged their plague content using a qPCR assay targeting the bacterium's pla gene. Based on this, they had 53 positive extracts from 32 people, though only three — one from each site — had enough Y. pestis DNA for further analysis.

Using a whole-genome array capture based on Y. pseudotuberculosis and the Y. pestis plasmids, the researchers obtained average genomic coverage of 10.3-fold for the Barcelona sample, 19.3-fold for the Bolgar City, and 4.9-fold for the Ellwangen sample.

With these samples along with 141 modern Y. pestis genomes — including ones from the former Soviet Union — and seven other historical genomes, the researchers constructed a Y. pestis phylogeny. It revealed that all three of the newly analyzed historical samples belonged to the same branch of the plague phylogenetic tree and housed SNPs previously found in Black Death samples.

There were no differences between the Barcelona Black Death strain analyzed here and three previously genotyped strains from London from between 1348 and 1350, Spyrou and her colleagues reported. Barcelona, they added, is thought to be one of the main entry points for the Black Death into Europe with historical records indicating its introduction there in the spring of 1348 and reaching London by the fall of that year. The analysis, they added, suggests that the Black Death strain had low genetic diversity and may have entered Europe in a single wave.

The Bolgar City sample, meanwhile, exhibited differences at four genomic positions, two of which are shared by a London sample from the late 14th century, one of which is shared by all modern strains, and one of which is unique to that sample. This indicates that a plague strain circulating in London traveled eastward to Russia, and from there may have extended to China to give rise to more recent epidemics, the researchers said.

Additionally, the Ellwangen sample fell within a sub-branch related to the Barcelona and London strains that also includes strains from an outbreak in Marseilles from 1720 to 1722. The Ellwangen sample shared 20 positions with those samples from Marseilles and had three unique SNPs, suggesting a common origin and a likely split before the Ellwangen outbreak in the 16th century. According to the researchers, this finding supports the notion that there was a European reservoir of the disease, such as a rodent.

Overall, the researchers said that their findings indicate that the Black Death arrived in the Mediterranean, spread to Northern Europe, and traveled east to Russia and then to China. Along the way, some strains like the Marseilles and Ellwangen ones were left behind to diversify and cause later epidemics.