Introduction
Lyme borreliosis (LB), also termed Lyme disease, is the most common
vector-borne disease in the Northern hemisphere (Stanek et al., 2011;
Steere, Coburn, & Glickstein, 2004), caused by certain genospecies ofBorrelia bacteria (Kurtenbach et al., 2006; Gabriele Margos,
Fingerle, & Reynolds, 2019; Stanek et al., 2011). These spirochete
bacteria are maintained naturally in obligatory transmission cycles
between tick vectors and specific vertebrate reservoir hosts (Kurtenbach
et al., 2006). In North America human LB is predominantly caused byBorrelia burgdorferi sensu stricto (Bb ss) while three
additional genospecies act as causative agents across Eurasia
(Borrelia afzelii , Borrelia bavariensis , Borrelia
garinii ) (Kurtenbach et al., 2006; Gabriele Margos et al., 2019; Stanek
et al., 2011). Genomic analyses have already shown a complex ancestral
spread of Bb ss across North America (Walter, Carpi, Caccone, &
Diuk-Wasser, 2017) which is also observed in specific Eurasian
genospecies (Becker et al., 2020; Ana Cláudia Norte et al., 2020). The
Eurasian genospecies offer a unique opportunity to understand the
geographic expansion of Borrelia spirochetes using comparative
genomics. However, no study has integrated genomic data from the
different genospecies. In particular, no study at the population-level
of Asian B. afzelii has been published to date.
Borrelia genospecies cannot transmit successfully through all
tick species (Eisen, 2020; Gabriele Margos et al., 2019) and can only
infect specific vertebrate classes (i.e. rodents, passerines, sea-birds,
etc.) while being easily cleared by the immune systems of others
(Kurtenbach et al., 2006; Kurtenbach, Sewell, Ogden, Randolph, &
Nuttall, 1998; Gabriele Margos et al., 2019). Eurasian Borreliagenospecies currently exist in separate transmission cycles vectored
predominately by two generalist tick species in Asia (Ixodes
persulcatus ) and Europe (Ixodes ricinus ) (Kurtenbach et al.,
2006) (Figure 1). This suggests that each genospecies successfully
invaded a novel tick vector resulting in the expansion into a new
continental transmission cycle. However, how and in which order this
expansion occurred is still unknown (Figure 1). For B.
bavariensis, an Asian origin was already hypothesized as the Asian
population displays a higher genetic diversity compared to the almost
clonal European population (Becker et al., 2020; Gatzmann et al., 2015;
Gabriele Margos et al., 2019). European B. bavariensis is thought
to have undergone a selective bottleneck while colonizing the European
tick vector, I. ricinus , resulting in the observed clonal
structure (Becker et al., 2020; Gatzmann et al., 2015; Gabriele Margos
et al., 2019). Whether or not the other genospecies also underwent this
bottleneck has never been studied so far. Both B. afzelii andB. bavariensis utilize rodents as reservoir hosts (Pär Comstedt,
Jakobsson, & Bergström, 2011; Kurtenbach et al., 2006; Gabriele Margos
et al., 2009) (Figure 1). In comparison, B. garinii is adapted to
avian host species (Pär Comstedt et al., 2009, 2011), which includes
interconnected terrestrial and marine transmission cycles (Figure 1).
This association in B. garinii is thought to allow for migration
between the European and Asian populations which is not accessible to
rodent adapted genospecies. (Figure 1).
Each of these genospecies has successfully established into multiple
transmission cycles and offers an opportunity to study howBorrelia expanded across Eurasia through comparative genomics.
Although, no study to date has integrated genomic data from all three
Eurasian-distributed genospecies. Here we report the reconstructed
evolutionary history of 142 B. afzelii , B. garinii , andB. bavariensis Eurasian isolates based on full genome sequences
including the first Japanese B. afzelii genomes sequenced. Our
results highlight that these genospecies share an Asian origin with
support for migration from an ancestral Asian population vectored byI. persulcatus into a novel European vector, I. ricinus .
Post-colonization gene flow appears to be associated with the dispersal
range of the respective reservoir host species. Our results provide new
information on the ability of three Borrelia genospecies to
colonize new environments and how this could relate to the further
expansion of human LB.