Comparative population genomics of the Borrelia burgdorferi species complex reveals high degree of genetic isolation among species and underscores benefits and constraints to studying intra-specific epidemiological processes.

Maude Jacquot (1) , Mathieu Gonnet (1) , Elisabeth Ferquel (2) , David Abrial (1) , Alexandre Claude (1) , Patrick Gasqui (3) , Valérie Choumet (4) , Myriam Garrido (1) , Martine Garnier (2) , Benjamin Faure (1) , Natacha Sertour (2) , Nelly Dorr (1) , Jocelyn de Goër (1) , Gwenaël Vourc’h (1) , Xavier Bailly (1)

1 Unité d'épidémiologie animale
2 CNR - Centre National de Référence des Borrelia
3 UR EpiA - Unité de Recherche d'Épidémiologie Animale
4 Interactions Moléculaires Flavivirus-Hôtes

Lyme borreliosis, one of the most frequently contracted zoonotic diseases in the Northern Hemisphere, is caused by bacteria belonging to different genetic groups within the Borrelia burgdorferi species complex, which are transmitted by ticks among various wildlife reservoirs, such as small mammals and birds. These features make the Borrelia burgdorferi species complex an attractive biological model that can be used to study the diversification and the epidemiology of endemic bacterial pathogens. We investigated the potential of population genomic approaches to study these processes. Sixty-three strains belonging to three species within the Borrelia burgdorferi complex were isolated from questing ticks in Alsace (France), a region where Lyme disease is highly endemic. We first aimed to characterize the degree of genetic isolation among the species sampled. Phylogenetic and coalescent-based analyses revealed clear delineations: there was a ∼50 fold difference between intra-specific and inter-specific recombination rates. We then investigated whether the population genomic data contained information of epidemiological relevance. In phylogenies inferred using most of the genome, conspecific strains did not cluster in clades. These results raise questions about the relevance of different strategies when investigating pathogen epidemiology. For instance, here, both classical analytic approaches and phylodynamic simulations suggested that population sizes and migration rates were higher in B. garinii populations, which are normally associated with birds, than in B. burgdorferi s.s. populations. The phylogenetic analyses of the infection-related ospC gene and its flanking region provided additional support for this finding. Traces of recombination among the B. burgdorferi s.s. lineages and lineages associated with small mammals were found, suggesting that they shared the same hosts. Altogether, these results provide baseline evidence that can be used to formulate hypotheses regarding the host range of B. burgdorferi lineages based on population genomic data.

Mots clés: FREQUENCY-DEPENDENT SELECTION; SENSU-LATO; LYME BORRELIOSIS; DIFFERENTIAL TRANSMISSION; PHYLOGENETIC NETWORKS; SEQUENCE-ANALYSIS; RESERVOIR HOSTS; DIVERSITY

Mots clés: FINITE POPULATIONS; EVOLUTION

Domaines: Sciences du Vivant [q-bio]

Maude Jacquot, Mathieu Gonnet, Elisabeth Ferquel, David Abrial, Alexandre Claude, et al.. Comparative population genomics of the Borrelia burgdorferi species complex reveals high degree of genetic isolation among species and underscores benefits and constraints to studying intra-specific epidemiological processes.. PLoS ONE, 2014, 9 (4), pp.e94384. ⟨10.1371/journal.pone.0094384⟩. ⟨pasteur-01054563⟩