Evolutionary history of contagious bovine pleuropneumonia using next generation sequencing of Mycoplasma mycoides Subsp. mycoides "Small Colony".

Virginie Dupuy,François Poumarat,Marc Breton,Alain Blanchard,Valérie Barbe,Lucía Manso-Silván,Pascal Sirand-Pugnet,François Thiaucourt,Christine Citti,Emilie Dordet-Frisoni,Patricia Thebault

doi:10.1371/journal.pone.0046821

Abstract

Mycoplasma mycoides subsp. mycoides “Small Colony” (MmmSC) is responsible for contagious bovine pleuropneumonia (CBPP) in bovidae, a notifiable disease to the World Organization for Animal Health (OIE). Although its origin is not documented, the disease was known in Europe in 1773. It reached nearly world-wide distribution in the 19th century through the cattle trade and was eradicated from most continents by stamping-out policies. During the 20th century it persisted in Africa, and it reappeared sporadically in Southern Europe. Yet, classical epidemiology studies failed to explain the re-occurrence of the disease in Europe in the 1990s. The objectives of this study were to obtain a precise phylogeny of this pathogen, reconstruct its evolutionary history, estimate the date of its emergence, and determine the origin of the most recent European outbreaks. A large-scale genomic approach based on next-generation sequencing technologies was applied to construct a robust phylogeny of this extremely monomorphic pathogen by using 20 representative strains of various geographical origins. Sixty two polymorphic genes of the MmmSC core genome were selected, representing 83601 bp in total and resulting in 139 SNPs within the 20 strains. A robust phylogeny was obtained that identified a lineage specific to European strains; African strains were scattered in various branches. Bayesian analysis allowed dating the most recent common ancestor for MmmSC around 1700. The strains circulating in Sub-Saharan Africa today, however, were shown to descend from a strain that existed around 1810. MmmSC emerged recently, about 300 years ago, and was most probably exported from Europe to other continents, including Africa, during the 19th century. Its diversity is now greater in Africa, where CBPP is enzootic, than in Europe, where outbreaks occurred sporadically until 1999 and where CBPP may now be considered eradicated unless MmmSC remains undetected.

Highlights

Epizootic diseases have threatened cattle since their domestication
The objectives of this study were to construct a robust phylogeny for this pathogen, establish when the most recent common ancestor of all MmmSC strains appeared, determine whether contagious bovine pleuropneumonia (CBPP) existed in Africa or, more likely, it was imported from Europe during colonization, and find the origins of the CBPP outbreaks that occurred in Southern Europe in the last decades
The CBPP agent was estimated by BEAST to have emerged around 1700 AD

Summary

Introduction

Epizootic diseases have threatened cattle since their domestication. Two of them played a prominent role in the last three centuries: rinderpest and contagious bovine pleuropneumonia (CBPP), threatening the livelihood of whole populations [1] and hindering international cattle trade. While rinderpest has been successfully eradicated world-wide [2], CBPP is still present in many African countries. The spread of CBPP in Europe and throughout the world in the middle of the 19th century is well documented, little is known about its origin [3]. The earliest documents by ‘‘Testienne’’ and Scheuchzer do not contain precise descriptions that could be unequivocally linked to CBPP [4,5]. Historical documents on CBPP do not provide any indication regarding the date of appearance of the disease or whether it existed from time immemorial

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Conclusion