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A large-scale genomic approach affords unprecedented resolution for the molecular epidemiology and evolutionary history of contagious caprine pleuropneumonia.

Dupuy V, Verdier A, Thiaucourt F, Manso-Silván L - Vet. Res. (2015)

Bottom Line: A Bayesian approach was used to infer the first robust phylogeny of the species and to date the principal events of its evolutionary history.Finally, plausible scenarios were proposed to elucidate the evolution and dynamics of CCPP in Asia and Africa, though limited by the paucity of Mccp strains, particularly in Asia.This study shows how combining large-scale genomic data with spatial and temporal data makes it possible to obtain a comprehensive view of the epidemiology of CCPP, a precondition for the development of improved disease surveillance and control measures.

View Article: PubMed Central - PubMed

Affiliation: CIRAD, UMR CMAEE, F-34398, Montpellier, France. virginie.dupuy@cirad.fr.

ABSTRACT
Contagious caprine pleuropneumonia (CCPP), caused by Mycoplasma capricolum subsp. capripneumoniae (Mccp), is a devastating disease of domestic goats and of some wild ungulate species. The disease is currently spreading in Africa and Asia and poses a serious threat to disease-free areas. A comprehensive view of the evolutionary history and dynamics of Mccp is essential to understand the epidemiology of CCPP. Yet, analysing the diversity of genetically monomorphic pathogens, such as Mccp, is complicated due to their low variability. In this study, the molecular epidemiology and evolution of CCPP was investigated using a large-scale genomic approach based on next-generation sequencing technologies, applied to a sample of strains representing the global distribution of this disease. A highly discriminatory multigene typing system was developed, allowing the differentiation of 24 haplotypes among 25 Mccp strains distributed in six genotyping groups, which showed some correlation with geographic origin. A Bayesian approach was used to infer the first robust phylogeny of the species and to date the principal events of its evolutionary history. The emergence of Mccp was estimated only at about 270 years ago, which explains the low genetic diversity of this species despite its high mutation rate, evaluated at 1.3 × 10(-6) substitutions per site per year. Finally, plausible scenarios were proposed to elucidate the evolution and dynamics of CCPP in Asia and Africa, though limited by the paucity of Mccp strains, particularly in Asia. This study shows how combining large-scale genomic data with spatial and temporal data makes it possible to obtain a comprehensive view of the epidemiology of CCPP, a precondition for the development of improved disease surveillance and control measures.

No MeSH data available.


Related in: MedlinePlus

Bayesian inference ofMycoplasma capricolumsubsp.capripneumoniaeevolutionary history. The Maximum Clade Credibility tree resulted from BEAST analysis of the alignment of concatenated sequences of 47 coding sequences from 25 Mccp strains. Bayesian posterior probabilities higher than 0.9 are represented by a white circle. Age estimates are displayed for relevant nodes with the 95% highest probability density intervals in brackets. The scale is given in years before present. The branch corresponding to the outgroup (California Kid) was shortened, as indicated by parallel bars.
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Fig2: Bayesian inference ofMycoplasma capricolumsubsp.capripneumoniaeevolutionary history. The Maximum Clade Credibility tree resulted from BEAST analysis of the alignment of concatenated sequences of 47 coding sequences from 25 Mccp strains. Bayesian posterior probabilities higher than 0.9 are represented by a white circle. Age estimates are displayed for relevant nodes with the 95% highest probability density intervals in brackets. The scale is given in years before present. The branch corresponding to the outgroup (California Kid) was shortened, as indicated by parallel bars.

Mentions: A robust phylogeny of Mccp was reconstructed based on high-throughput genomic data of 25 selected Mccp strains (Table 1) and an Mcc outgroup. Among the 57 genes previously analysed for genotyping, a set of 47 coding sequences was retained, while pseudogenes were excluded (Additional file 1) to minimise molecular clock variation and homoplasy. After alignment of the sequences, robust trees were inferred based on 134 SNPs using both maximum likelihood (Additional file 7) and Bayesian (Figure 2) approaches. Tree topologies were identical for supported branches. The six genotyping groups described above (group A to group F) were retrieved as clusters supported by high node support values. They formed two major lineages. Lineage I included group A, present in East Africa, and group B, present in Central Africa. Lineage II comprised groups C, D, E and F and was divided into two sub-lineages. The first sub-lineage comprised groups C and D, representing Asian strains, while group E (representing strains from the Mediterranean Basin) and group F (comprising mainly strains from East Africa) were clustered in a second, heterogeneous sub-lineage. Divergence time for Mccp strains was estimated from the dated sequences using the flexible Bayesian phylogenetic analysis package BEAST (Figure 2). Bayes Factor tests indicated that the strict-clock model fitted the data better than the relaxed-clock model. In contrast, there was no substantial difference between population models. To exempt analyses from dependence on a pre-specified demographic model, the extended Bayesian skyline plot model was applied. The mean substitution rate for Mccp, estimated on 47 coding sequences, was 1.3 × 10−6 (substitutions per site per year). The MRCA of Mccp strains emerged 269 years ago (95% highest posterior densities (HPDs) intervals between 120 years and 736 years). Lineage II diverged around 230 years ago (95% HPDs: 104–633) and dissociated into two sub-lineages dated 202 (95% HPDs: 88–554) and 136 years ago (95% HPDs: 67–360) respectively, while lineage I diverged around 159 years ago (95% HPDs: 66–438). All genotyping groups except D were formed recently at almost the same period (between 19 and 222 years ago), with the most probable age being between 35 years (for group A) and 90 years (for group F). Indeed, group D is represented by a single strain (the only Chinese strain available so far) and, as long as the diversity of this group remains unresolved, it will not be possible to date its emergence.Figure 2


A large-scale genomic approach affords unprecedented resolution for the molecular epidemiology and evolutionary history of contagious caprine pleuropneumonia.

Dupuy V, Verdier A, Thiaucourt F, Manso-Silván L - Vet. Res. (2015)

Bayesian inference ofMycoplasma capricolumsubsp.capripneumoniaeevolutionary history. The Maximum Clade Credibility tree resulted from BEAST analysis of the alignment of concatenated sequences of 47 coding sequences from 25 Mccp strains. Bayesian posterior probabilities higher than 0.9 are represented by a white circle. Age estimates are displayed for relevant nodes with the 95% highest probability density intervals in brackets. The scale is given in years before present. The branch corresponding to the outgroup (California Kid) was shortened, as indicated by parallel bars.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4492101&req=5

Fig2: Bayesian inference ofMycoplasma capricolumsubsp.capripneumoniaeevolutionary history. The Maximum Clade Credibility tree resulted from BEAST analysis of the alignment of concatenated sequences of 47 coding sequences from 25 Mccp strains. Bayesian posterior probabilities higher than 0.9 are represented by a white circle. Age estimates are displayed for relevant nodes with the 95% highest probability density intervals in brackets. The scale is given in years before present. The branch corresponding to the outgroup (California Kid) was shortened, as indicated by parallel bars.
Mentions: A robust phylogeny of Mccp was reconstructed based on high-throughput genomic data of 25 selected Mccp strains (Table 1) and an Mcc outgroup. Among the 57 genes previously analysed for genotyping, a set of 47 coding sequences was retained, while pseudogenes were excluded (Additional file 1) to minimise molecular clock variation and homoplasy. After alignment of the sequences, robust trees were inferred based on 134 SNPs using both maximum likelihood (Additional file 7) and Bayesian (Figure 2) approaches. Tree topologies were identical for supported branches. The six genotyping groups described above (group A to group F) were retrieved as clusters supported by high node support values. They formed two major lineages. Lineage I included group A, present in East Africa, and group B, present in Central Africa. Lineage II comprised groups C, D, E and F and was divided into two sub-lineages. The first sub-lineage comprised groups C and D, representing Asian strains, while group E (representing strains from the Mediterranean Basin) and group F (comprising mainly strains from East Africa) were clustered in a second, heterogeneous sub-lineage. Divergence time for Mccp strains was estimated from the dated sequences using the flexible Bayesian phylogenetic analysis package BEAST (Figure 2). Bayes Factor tests indicated that the strict-clock model fitted the data better than the relaxed-clock model. In contrast, there was no substantial difference between population models. To exempt analyses from dependence on a pre-specified demographic model, the extended Bayesian skyline plot model was applied. The mean substitution rate for Mccp, estimated on 47 coding sequences, was 1.3 × 10−6 (substitutions per site per year). The MRCA of Mccp strains emerged 269 years ago (95% highest posterior densities (HPDs) intervals between 120 years and 736 years). Lineage II diverged around 230 years ago (95% HPDs: 104–633) and dissociated into two sub-lineages dated 202 (95% HPDs: 88–554) and 136 years ago (95% HPDs: 67–360) respectively, while lineage I diverged around 159 years ago (95% HPDs: 66–438). All genotyping groups except D were formed recently at almost the same period (between 19 and 222 years ago), with the most probable age being between 35 years (for group A) and 90 years (for group F). Indeed, group D is represented by a single strain (the only Chinese strain available so far) and, as long as the diversity of this group remains unresolved, it will not be possible to date its emergence.Figure 2

Bottom Line: A Bayesian approach was used to infer the first robust phylogeny of the species and to date the principal events of its evolutionary history.Finally, plausible scenarios were proposed to elucidate the evolution and dynamics of CCPP in Asia and Africa, though limited by the paucity of Mccp strains, particularly in Asia.This study shows how combining large-scale genomic data with spatial and temporal data makes it possible to obtain a comprehensive view of the epidemiology of CCPP, a precondition for the development of improved disease surveillance and control measures.

View Article: PubMed Central - PubMed

Affiliation: CIRAD, UMR CMAEE, F-34398, Montpellier, France. virginie.dupuy@cirad.fr.

ABSTRACT
Contagious caprine pleuropneumonia (CCPP), caused by Mycoplasma capricolum subsp. capripneumoniae (Mccp), is a devastating disease of domestic goats and of some wild ungulate species. The disease is currently spreading in Africa and Asia and poses a serious threat to disease-free areas. A comprehensive view of the evolutionary history and dynamics of Mccp is essential to understand the epidemiology of CCPP. Yet, analysing the diversity of genetically monomorphic pathogens, such as Mccp, is complicated due to their low variability. In this study, the molecular epidemiology and evolution of CCPP was investigated using a large-scale genomic approach based on next-generation sequencing technologies, applied to a sample of strains representing the global distribution of this disease. A highly discriminatory multigene typing system was developed, allowing the differentiation of 24 haplotypes among 25 Mccp strains distributed in six genotyping groups, which showed some correlation with geographic origin. A Bayesian approach was used to infer the first robust phylogeny of the species and to date the principal events of its evolutionary history. The emergence of Mccp was estimated only at about 270 years ago, which explains the low genetic diversity of this species despite its high mutation rate, evaluated at 1.3 × 10(-6) substitutions per site per year. Finally, plausible scenarios were proposed to elucidate the evolution and dynamics of CCPP in Asia and Africa, though limited by the paucity of Mccp strains, particularly in Asia. This study shows how combining large-scale genomic data with spatial and temporal data makes it possible to obtain a comprehensive view of the epidemiology of CCPP, a precondition for the development of improved disease surveillance and control measures.

No MeSH data available.


Related in: MedlinePlus