Early Divergent Strains of Yersinia pestis in Eurasia 5,000 Years Ago

Abstract

SummaryThe bacteria Yersinia pestis is the etiological agent of plague and has caused human pandemics with millions of deaths in historic times. How and when it originated remains contentious. Here, we report the oldest direct evidence of Yersinia pestis identified by ancient DNA in human teeth from Asia and Europe dating from 2,800 to 5,000 years ago. By sequencing the genomes, we find that these ancient plague strains are basal to all known Yersinia pestis. We find the origins of the Yersinia pestis lineage to be at least two times older than previous estimates. We also identify a temporal sequence of genetic changes that lead to increased virulence and the emergence of the bubonic plague. Our results show that plague infection was endemic in the human populations of Eurasia at least 3,000 years before any historical recordings of pandemics.

How old are bacterial pathogens?

“…Bronze-age genomes of this pathogen were found in both Poland and Russia [31], and each of the last three pandemics has swept across large parts of Eurasia. Thus, plague caused by Y. pestis has swept across Asia on multiple occasions over the last 5000 years, or even longer.…”

“…Branches and populations within that tree that are defined by extant diversity have already been assigned characteristic names [16,30,48], for example branch 0 for the ancestral branch leading from [30], [16] and [31], including additional ancient genomes and genotypes (see below), plus proposed mnemonics for those populations. Sources of ancient genomes and genotypes: the Bronze Age (0.PRE1, 0.PRE2; grey) [31], the Justinianic Pandemic (0.ANT4; blue) [32]; the Black Death (1.PRE1; maroon; London, 1348 [33]; Barcelona 1300-1420 [34]; SNP-based genotypes from Germany (fourteenth and seventeenth centuries) [35]) and descendent branches of 1.PRE from Ellwangen (1.PRE1B; 1485-1627) [34] and Marseille (1.PRE1.A, 1722) [36]). One SNP further along branch 1 are the populations 1.PRE2 (London, 1362-1400 [36] and the related low-resolution genotype found in Berg-Op-Zoom, The Netherlands from the fourteenth century [37]; green).…”

“…One further SNP down the branch is a short branch leading to a genome from Western Asia (1.PRE3; Bolgar City, Tatarstan, Russia; light blue) [34]. Branch 0 begins with ancient genomes from the teeth of Bronze-age individuals who died up to 5000 years ago [31] (populations 0.PRE1, 0.PRE2). These are followed by a variety of extant populations found today in eastern and central Asia (0.PE7, 0.PE1-4, 0.ANT1) [16,30] and then by a genome from the Justinianic pandemic in Germany (0.ANT4) [32].…”

Reproductive trade-offs in extant hunter-gatherers suggest adaptive mechanism for the Neolithic expansion

“…Research reveals increased prevalence of tuberculosis, syphilis, and the plague (6,(23)(24)(25), overall immunological stress (26), and a deterioration in oral health (16,27,28). Farming led to higher population densities, sedentarization, increased contact with neighboring populations, the presence of rodents attracted by food stores, the domestication of animals, and fecal pollution (29)(30)(31).…”

Genomic Analysis of Bacterial Outbreaks

“…But the methods are also valid for more slowly evolving organisms with sampling dates different enough as to provide estimates of the evolutionary rate. Recently, this approach has been used with bacterial genomes obtained from ancient samples (Schuenemann et al, 2013;Bos et al, 2014;Mendum et al, 2014;Rasmussen et al, 2015;Bos et al, 2016;Maixner et al, 2016).…”