Comparison of French and Worldwide Bacillus anthracis Strains Favors a Recent, Post-Columbian Origin of the Predominant North-American Clade

Abstract

BackgroundBacillus anthracis, the highly dangerous zoonotic bacterial pathogen species is currently composed of three genetic groups, called A, B and C. Group A is represented worldwide whereas group B is present essentially in Western Europe and Southern Africa. Only three strains from group C have been reported. This knowledge is derived from the genotyping of more than 2000 strains collected worldwide. Strains from both group A and group B are present in France. Previous investigations showed that the majority of sporadic French strains belong to the so-called A.Br.011/009 group A clade and define a very remarkable polytomy with six branches. Here we explore the significance of this polytomy by comparing the French B. anthracis lineages to worldwide lineages. We take advantage of whole genome sequence data previously determined for 122 French strains and 45 strains of various origins.ResultsA total of 6690 SNPs was identified among the available dataset and used to draw the phylogeny. The phylogeny of the French B group strains which belongs to B.Br.CNEVA indicates an expansion from the south-east part of France (the Alps) towards the south-west (Massif-Central and Pyrenees). The relatively small group A strains belonging to A.Br.001/002 results from at least two independent introductions. Strikingly, the data clearly demonstrates that the currently predominant B. anthracis lineage in North America, called WNA for Western North American, is derived from one branch of the A.Br.011/009 polytomy predominant in France.Conclusions/SignificanceThe present work extends the range of observed substitution rate heterogeneity within B. anthracis, in agreement with its ecology and in contrast with some other pathogens. The population structure of the six branches A.Br.011/009 polytomy identified in France, diversity of branch length, and comparison with the WNA lineage, suggests that WNA is of post-Columbian and west European origin, with France as a likely source. Furthermore, it is tempting to speculate that the polytomy’s most recent common ancestor -MRCA- dates back to the Hundred Years' war between France and England started in the mid-fourteenth century. These events were associated in France with deadly epidemics and major economic and social changes.

Insights from Bacillus anthracis strains isolated from permafrost in the tundra zone of Russia

“…Figure 4 shows the structure of the A.Br.011/009 polytomy, using the fifty-four read archives or genome assemblies assigned to A.Br.011/009. The polytomy comprises six branches numbered L1 to L6 in agreement with previous reports [37, 38]. The monophyletic A.Br.WNA lineage exclusively present and predominant in North-America emerged from A.Br.011/009_L2 and is represented by four strains in Figure 4 [28, 38–40].…”

“…The polytomy comprises six branches numbered L1 to L6 in agreement with previous reports [37, 38]. The monophyletic A.Br.WNA lineage exclusively present and predominant in North-America emerged from A.Br.011/009_L2 and is represented by four strains in Figure 4 [28, 38–40]. Interestingly, the WNA lineage is branching from the Canadian strain A0303 which shows the ancestral state for the A.Br.WNA canSNP, i.e.…”

“…Consequently, the analysis of currently available A.Br.011/009 sequencing data strengthens the previously reported view of the A.Br.011/009 polytomy, characterized by a limited geographic distribution of the “slowly evolving” lineages contrasting with the very fast expanding lineages observed in West Africa and North America [38]. After the North American-West African split shown in Figure 4, French strains from lineage L2 expanded for a further 15 to 22 SNPs when not including two strains obtained from the Collection de l’Institut Pasteur (CIP) which might have been extensively cultivated and define slightly longer branches.…”

“…Lineages L5 and L6 each contain a single deep branching lineage, observed in Turkey. The last lineage leads to TEA Br011 corresponding to the A.Br.011/009 polytomy [37, 38] found in France. In summary, eleven deep-branching lineages are detected within the seven-branch TEA 008/011 polytomy, nine of which with a strong geographic assignment, to Turkey (2), China (2), Russia (2, including Northern Yakutia, Siberia), Italy, Bulgaria and France.…”

“…The color coding reflects the lineages within the A.Br.011/009 polytomy using the previously defined classification [38]. Within L3, strains derived from the Pasteur II vaccine are colored in pink.…”