How a microbe becomes a pandemic: a new story of the Black Death

In 2011, palaeogeneticists at McMaster University, Canada, and Tübingen University, Germany, reconstructed the genomes of Yersinia pestis, the causative organism of plague, from two 14th-century cemeteries below the centre of London.1Bos KI Schuenemann VJ Golding GB et al.A draft genome of Yersinia pestis from victims of the Black Death.Nature. 2011; 478: 506-510Crossref PubMed Scopus (432) Google Scholar, 2Bos KI Herbig A Sahl J et al.Eighteenth century Yersinia pestis genomes reveal the long-term persistence of an historical plague focus.eLife. 2016; 5e12994Crossref PubMed Google Scholar Since then, the Black Death and subsequent outbreaks of plague have been documented by additional genetic material—aDNA—retrieved from gravesites throughout Europe and southern Russia dating from the 14th to 18th centuries. One story this aDNA tells is that the most important event in plague history was not the Black Death, but something that preceded it: the Big Bang. The Big Bang is the eponym for a major divergence—a polytomy—that occurred in the evolution of Y pestis sometime before the Black Death. The date of the Big Bang is constrained by the aDNA. It cannot be younger than the London Black Death Cemetery's foundation (1348) and closure (1350), and it is unlikely to be older than the postulated limits, from the 10th to the early-14th century, derived from molecular clock analyses. That is still a wide margin of uncertainty, however. To pinpoint a so-called event in the history of a microbe, the cause of a rodent disease, might seem a fool's errand. Yet plague, as is well known, is not just a disease of rodents. It kills a lone shepherd here, an isolated huntress there. Most of those deaths are lost forever to history, the fate of anonymity befalling most people of the past. But at other times, plague proliferates fulminously. Reports of deaths numbering 1000 or more per day are not uncommon in medieval sources describing urban outbreaks. Beyond a particular threshold, plague leaves an indelible mark on the record of human history. The genome of Y pestis, like that of all organisms, carries indelible marks. Its single nucleotide polymorphisms (SNPs) allow researchers to join the history of this horrifically lethal microbe to the history of human activities that have facilitated its transport and replication. An alliance of genetics and old-fashioned historical inquiry has made it possible to identify both the presumed locus and the causal circumstances of the Big Bang. To the identification of the pathogenic cause of the Black Death, which was confirmed in 2011, a human cause can now be added. The living Y pestis strains most closely related to those implicated in late-medieval Europe's Black Death are found in marmots, hibernating animals that normally live far from human habitation. Yet the marmots carrying these closely related strains are found nowhere near Europe. Rather, they are tightly clustered in adjacent habitats in and near the Tian Shan mountain range, on the eastern border of Kyrgyzstan. The lineages of Y pestis that are hosted in Tian Shan marmots are, moreover, living relatives of at least three other lineages descended from the Big Bang. This late-medieval proliferation scattered new plague lineages in every direction around the Tian Shan, taking the bacterium into marmot populations separated by 1000 km or more. The marmots themselves are all different species than the ancestral host of Y pestis. To the historian, such a remarkable constellation of dispersal conjures up not environmental accidents or rodent migrations, but human disruptions. And in that time and in that place—central Asia in the century before the Black Death—one group was a notably disruptive force: the Mongols. The Mongol Empire (1206–1368) was the largest land empire in human history. To date, historiography has barely associated the Mongols with plague, save for the now-discredited fiction that they spread the Black Death to Europe by throwing plague-ridden bodies over the walls during a siege of Caffa on the Black Sea.3Barker H Laying the corpses to rest: grain, embargoes, and Yersinia pestis in the Black Sea, 1346–1348.BodoArXiv. 2020; (published online May 2.) (preprint)https://doi.org/10.34055/osf.io/rqn8hGoogle Scholar The spread of plague in the 1340s was hardly an act of bioterrorism; instead, its introduction into the commercial routes of the Black Sea and Mediterranean was due to grain shipments unrelated to the siege. The same mundane activity is probably what dispersed plague across central Asia, a century before the Black Death as has usually been described.4Green MH The four Black Deaths.Am Hist Rev. 2020; 125: 1600-1631Google Scholar The Big Bang was a spillover event. The marmots that still carry pre-polytomy strains of plague in the Tian Shan probably served as sources of food, furs, and leather for the Mongol armies when they descended out of Mongolia. In the foothills of the Tian Shan mountains, Mongol supply chains gathered up grain to feed their campaigning troops, particularly a kind of millet unique to the region. Sacks of grain were then transported to the fortresses and cities where the Mongols laid their greatest sieges between the 1210s and the 1250s, as far distant as Kaifeng in China and Baghdad in Persia. Something so insignificant as a few sacks of millet, into which a few plague-infected rodents crawled, might account for the worst scenes of human suffering the world has witnessed. This story has been reconstructed because, in the past decade, genetics laid a trail of breadcrumbs for historians, who were alert enough to pick it up. The SNPs used to derive the phylogeny of Y pestis were clues, shifting historians’ focus away from the Black Sea to an entirely different part of Eurasia. Geneticists’ speculations about the date of the Big Bang likewise induced historians to look a century earlier for evidence of plague. The SNPs brought attention to the marmots and the realisation that they harbour strains of plague extremely close to the Big Bang. What unites historical pandemic events is not the type of pathogen. It is human agency.5Green MH Emerging diseases, re-emerging histories.Centaurus. 2020; 62: 238-251Crossref Scopus (10) Google Scholar Our choices in food acquisition, our networks of commodity distribution, our drive for cheap labour or for sex—all have turned small outbreaks and spillover events into global scourges. As the WHO prepares to search for the origin of the COVID-19 pandemic, it might reveal more than zoonotic spillover. It will probably reveal a familiar sequence of humans doing what humans do. Maybe these stories have no villains. Maybe they are as mundane as microbes in a sack of grain. I declare no competing interests.

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