Achtman on Plague Evolution

Mark Achtman who led the international team that assembled the phylogenetic tree for Yersinia pestis participated in a Royal Society meeting on ‘Immunity, infection, migration and human evolution’ in June 2011. Achtman’s contribution placed plague evolution within the context of other ‘monomorphic’ pathogens.

Here are some of my notes from his published contribution:

  • Monomorphic pathogens like Yersinia pestis emerge as clones of more diverse pan-genomic species that are adapted to a wide environmental niche. After a phase of rapid natural selection to fit to a new niche, the clone becomes isolated and evolves almost exclusively by mutation alone. Horizontal gene transfer is extremely rare in monomorphic species, although plasmids and bacteriophages are sometimes acquired.
  • The short period of adaption in the new niche will probably be invisible in existing clones and aDNA. After the initial niche fitting, they undergo a mild purifying selection or neutral evolution that makes them less diverse than the average bacterial species. Achtman notes that transmission to humans represents  a genetic bottleneck that would further restrict diversity.
  • Mutation clock rates must be set for every species. Trends show that the longer the time range examined the slower the clock rate. When rates are examined over shorter periods, the rates tend to be faster. This suggests to me that these rates are not consistent, perhaps changing speeds over time.  The clock for Yersinia pestis was set by samples collected over 70 years in Madagascar. I seem to recall buried in the supplemental material of Morelli et al (2010) they opened the possibility that mutation clock rates may not run at the same rate during epidemic and endemic periods. This is a big caveat on the clock rates.
  • Plague originated in Central Asia (former Soviet Union, Mongolia, China). Rat fleas have specifically been implicated in transmission in India  and Madagascar during the third pandemic. Achtman calls rats “secondary hosts” and possibly not relevant to plague evolution. Likewise, human epidemics are “accidental”.

I’ve redesigned the phylogenetic tree given in Achtman, 2012 and the original paper, Morelli et al, 2010 below so that it works better online and is hopefully easier to read. This diversity is based primarily on single nucleotide polymorphisms (SNPs), similar to genetic fingerprints that usually do not affect function. The right branch (branch 2) of including the ‘medievalis’ isolates (2.Med1 and 2.Med2) evolved along the Silk Road after the Black Death. The left branch is much more diverse including Antiqua strains (1.Ant1) that are closest to the root species. The far left cluster of ‘orientalis’ strains (1.Ori1-3) represent the global spread of the third pandemic. The dates given here come from Acthman (2012), and may be a bit optimistic.

Major branches of the Yersinia pestis pedigree. ya= years ago. Not to scale, after Achtman, 2012 and Morelli et al, 2010.
Table showing the 18 genetic changes that differentiate the branches of Yersinia pestis along with some aDNA results from Haensch et al, 2010.
  • Achtman places the genotypes from Black Death skeletons (aDNA) at the beginning of branch 1 but the figure places it at the branch point between branch 1 and 2. Haensch et al (2010) show the samples from Hereford England and Saint- Laurent-de-la-Cabrerisse France placed the Black Death at the branch point between the first and second branch (as indicated above). Another sample taken from the 14th century Netherlands was further up the first branch.
  • Achtman suggests that the Plague of Justinian, based on its date could have been closest to 0.PE3 since 0.PE4 is not found in large mammals. Note Haensch et al (2010) display 0.PE3 as a point on the main stem.
  • Achtman strongly places the origin of Yersinia pestis in China rather than elsewhere in Central Asia. The second branch (2.MED) correlates very well with the path of the Silk Road. Achtman also suggests that the 1.ANT1 clones were taken to East Africa in the 15th century. They persist in linking it with the voyage of Zheng He in the early 15th century, but I am hesitant to associate it with a particular voyage without more information. It is likely that other traders were following a similar path between the Indian Ocean and Eastern Africa.
  • Populations correlate well with geography. The spread of the third pandemic can be plotted with by using samples of the populations of the first branch. Plotting the other branches with the geographic locations also produces reliable trends.
  • Achtman (2012:865) concludes that “evolution of novel microbial pathogens is a very rare event, and increased levels of disease are more likely to reflect environmental changes than evolutionary adaption.”

References:

Achtman, M. (2012). Insights from genomic comparisons of genetically monomorphic bacterial pathogens Philosophical Transactions of the Royal Society B: Biological Sciences, 367 (1590), 860-867 DOI: 10.1098/rstb.2011.0303

Morelli G, Song Y, Mazzoni CJ, Eppinger M, Roumagnac P, Wagner DM, Feldkamp M, Kusecek B, Vogler AJ, Li Y, Cui Y, Thomson NR, Jombart T, Leblois R, Lichtner P, Rahalison L, Petersen JM, Balloux F, Keim P, Wirth T, Ravel J, Yang R, Carniel E, & Achtman M (2010). Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nature genetics, 42 (12), 1140-3 PMID: 21037571

Haensch S, Bianucci R, Signoli M, Rajerison M, Schultz M, Kacki S, Vermunt M, Weston DA, Hurst D, Achtman M, Carniel E, & Bramanti B (2010). Distinct clones of Yersinia pestis caused the black death. PLoS pathogens, 6 (10) PMID: 20949072

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