A novel Borrelia species, intermediate between Lyme disease and relapsing fever groups, in neotropical passerine-associated ticks

Abstract

Lyme disease (LD) and relapsing fevers (RF) are vector-borne diseases caused by bacteria of the Borrelia genus. Here, we report on the widespread infection by a non-described Borrelia species in passerine-associated ticks in tropical rainforests of French Guiana, South America. This novel Borrelia species is common in two tick species, Amblyomma longirostre and A. geayi, which feed on a broad variety of neotropical mammal and bird species, including migratory species moving to North America. The novel Borrelia species is divergent from the LD and RF species, and is more closely related to the reptile- and echidna-associated Borrelia group that was recently described. Genome sequencing showed that this novel Borrelia sp. has a relatively small genome consisting of a 0.9-Mb-large chromosome and an additional 0.3 Mb dispersed on plasmids. It harbors an RF-like genomic organization but with a unique mixture of LD- and RF-specific genes, including genes used by RF Borrelia for the multiphasic antigen-switching system and a number of immune-reactive protein genes used for the diagnosis of LD. Overall, our data indicate that this novel Borrelia is an intermediate taxon between the LD and RF species that may impact a large host spectrum, including American mammals. The designation "Candidatus Borrelia mahuryensis" is proposed for this species.

Figure 1

Location of sampling sites in French Guiana. Localities are represented by dots, and numbers correspond to the sampling site number given in Table S1. A letter placed after number indicates a same sampling site sampled over several years as detailed in Table S1. Red and black dots indicate populations infected by Cand. Borrelia mahuryensis and populations not infected, respectively. Bar-charts represents the prevalence of Cand. Borrelia mahuryensis in the sites where infected ticks were collected. Pictures to the left represents a female Crimson-hooded Manakin (Pipra aureola) bearing ticks around its eyes and a nymph of the tick species Amblyomma longirostre.

Figure 2

The network of ticks, passerines, and Cand. Borrelia mahuryensis. Each red node (with letters) and each black node (with numbers) designate a tick and passerine species, respectively. Solid edges indicate pairs of tick/passerine species for which Cand. Borrelia mahuryensis was detected (see Table S1 for details). (A) Amblyomma longirostre; (B) A. geayi; (C) A. varium; (D) A. cajennense; (E) A. calcaratum; (F) A. humerale; 1, Attila spadiceus; 2, Campylopterus largipennis; 3, Chiroxiphia pareola; 4, Cyanocompsa cyanoides; 5, Dendroplex picus; 6, Glyphorynchus spirurus; 7, Manacus manacus; 8, Mionectes macconnelli; 9, M. oleaginous; 10, Myrmeciza ferruginea; 11, Myrmotherula axillaris; 12, Percnostola rufifrons; 13, Picumnus exilis; 14, Pipra aureola; 15, P. erythrocephala; 16, Ramphocelus carbo; 17, Saltator maximus; 18, Thamnomanes caesius; 19, Thamnophilus doliatus; 20, T. punctatus; 21, Tolmomyias sulphurescens; 22, Turdus albicollis; 23, T. fumigatus; 24, T. leucomelas; 25, Xenops minutus; 26, Xiphorhynchus pardalotus.

Figure 3

Phylogenetic relationship of Borrelia species and strains estimated using maximum likelihood analysis of flaB gene sequences (323 unambiguously aligned bp). In red, sequences of Cand. Borrelia mahuryensis obtained in this study. Branch numbers indicate percentage bootstrap support (1,000 replicates).

Figure 4

Phylogenetic relationship of 19 Borrelia genomes, including the Cand. Borrelia mahuryensis A-FGy1 genome (in red). The phylogenetic tree was inferred using maximum likelihood analysis of a concatenated alignment of 590 single-copy orthologous genes (197,675 AA). The numbers on each node represent the support of 1,000 bootstrap replicates.

Figure 5

Whole-genome comparison of the pan-genome of the 19 Borrelia species and strains used in Fig. 4. Presence of a gene in a genome is indicated in black. The core genome of 638 genes and the genes unique to LD, RF, and third groups are clustered together in the heat map.