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Multiple Plague Pathogen Introductions to Europe Proposed by Genomic, Other Evidence

NEW YORK – The plague-causing Yersinia pestis pathogen appears to have been introduced to Europe multiple times during the so-called second plague pandemic between the mid-1300s and the end of the 19th century, according to a new genomic analysis by investigators in Norway, Italy, and China.

"Over the last few years, there has been a great deal of scientific debate regarding whether the plague bacterium, Yersinia pestis, spread from a Western European reservoir during the second plague pandemic, or if it repeatedly came to Europe from Asia," first and co-corresponding author Barbara Bramanti, a researcher affiliated with the University of Oslo's Center for Ecological and Evolutionary Synthesis and the University of Ferrara's neuroscience and rehabilitation department, and her colleagues wrote in a study published in the Proceedings of the National Academy of Sciences on Tuesday.

When they re-analyzed available genome sequence data for nearly 500 present-day Y. pestis isolates and more than 100 ancient representatives published in past studies and sequence databases, along with non-genetic evidence, the investigators found more support for the hypothesis that Y. pestis bacteria came to Europe repeatedly over the second plague pandemic, rather than residing in a Western European reservoir.

"[W]e make a synthesis of the available evidence, including genomes of ancient DNA and historical, archeological, and ecological information," the authors reported. "We conclude that the bacterium most likely came to Europe from Asia several times during the second plague pandemic."

For the analysis, the team focused on genome sequences for 111 ancient isolates, including almost four dozen from Western Europe, as well as 499 sequences for modern Y. pestis isolates. In the resulting phylogenetic tree, pathogen strains linked to the "Black Death" plague clustered together as a subset of isolates pinned to the broader second plague pandemic.

When they considered the genetic data in the context of ecological, epidemiological, archeological, historical, and evolutionary insights, the researchers saw examples of outbreaks that did not fit with the Western European reservoir hypothesis. In contrast, they reported, the data at hand tracked more closely with the notion that there were multiple Y. pestis plague introductions from Asia or Eastern Europe via rats, humans, trade goods, or other sources.

"This implies that there must have existed a reservoir outside of Western Europe [with the Ottoman Empire, Persia, and Central Asia as possible candidates]," the authors reported. "Such a reservoir could then feed, with multiple introductions, the second plague pandemic outbreaks in Western Europe along Northern and Southern trade routes."

The authors also saw hints that virulence of Y. pestis may have waned somewhat as historical plague pandemics started coming to a close, through convergent alterations affecting the plasmid-borne pla gene and other pathogen sequences.

"After experiencing the Black Death and successive waves, the pla decay strains might have attempted to acquire a fitness advantage, reducing their virulence by increasing the time to [host] death," the authors proposed. Even so, they noted that "the possible virulence reduction caused by pla decay and loss of the 49-[kilobase] region is not necessarily the reason for the extinction of plague at the end of the first and second pandemics but might be the result of a form of adaptation to a new host ... as well as their vectors."

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