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

Abstract

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.

Host dispersal shapes the population structure of a tick‐borne bacterial pathogen

“…The results presented in this study demonstrate how B. burgdorferi s.l.‐ vector‐ host associations and the behaviour of hosts may shape and impact the spread and dispersal, and ultimately the evolutionary biology of B. burgdorferi s.l., used here as a model for tick‐borne pathogens. Our data which includes B. garinii MLST characterization from bird‐derived ticks from the largest geographical range investigated so far substantiates that bird migration and dispersal movements appear to be one of the main driving forces to shape B. garinii populations, one of the most genetically heterogeneous Lyme borreliosis‐ causing genospecies (Jacquot et al, ; Margos et al, ). Because birds are highly mobile and the main reservoir hosts not only for B. garinii, but also for other pathogens, they contribute to frequent, fast and long‐range spatial mixing of strains and populations.…”

Vector potential and population dynamics for Amblyomma inornatum

“…A sequence related to the B. burgdorferi species complex was detected in 26/70 (37%) of the A. inornatum samples. B. burgdorferi is a species complex with a large number of closely related organisms (Jacquot et al 2014, Margos et al 2011). The clades within this complex often correspond to different host specificities (Brisson et al 2008, Margos et al 2011).…”

High conservation combined with high plasticity: genomics and evolution of Borrelia bavariensis

“…A similar discrepancy has also been shown at the level of the B. burgdorferi s.l. species complex [76] .…”