https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7327063/
A novel Borrelia species, intermediate between Lyme disease and relapsing fever groups, in neotropical passerine-associated ticks
Florian Binetruy,1 Stéphane Garnier,2 Nathalie Boulanger,3,4 Émilie Talagrand-Reboul,3,4 Etienne Loire,5 Bruno Faivre,2 Valérie Noël,1 Marie Buysse,1 and Olivier Duroncorresponding author1
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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.
Subject terms: Bacteria, Pathogens
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Introduction
Bacteria of the genus Borrelia (Spirochaetes) are the causative agents of major vector-borne diseases including Lyme disease (LD), the most important tick-borne disease in the northern hemisphere, and relapsing fevers (RF), which are transmitted by ticks and lice worldwide1,2. While RF epidemics occurred repeatedly in past centuries2, LD is an expanding infectious disease with more than 300,000 new human cases each year in the United States3,4. Most LD and RF Borrelia species are maintained in enzootic cycles and their presence in humans and domestic animals is incidental to their usual wildlife reservoir hosts1,2,5.
The LD and RF Borrelia species form two separate sister groups6,7, and are sometimes referred to as two sister genera by various authors8,9. LD and RF species were usually thought to be the only two groups within Borrelia. However, recent surveys have uncovered new Borrelia species and strains that do not fall into the LD or RF groups10–21. They form a third group, sometimes referred to as “reptile group” (REP), encompassing only two designated species, B. turcica and “Candidatus Borrelia tachyglossi” (B. tachyglossi hereafter), and a few strains not taxonomically described10–21. The only two genomes sequenced to date confirmed that these Borrelia are substantially different from the LD and RF Borrelia groups19. Members of the third Borrelia group have been detected worldwide, but not in Western Europe10–14,17,20,21. They have been detected in hard ticks (Amblyomma, Hyalomma, Bothriocroton, and Ixodes genera), which are associated mostly with reptiles, but also with echidna10–14,20,21. Recently, new strains of unknown Borrelia species, closely related to the third Borrelia group, were identified in ticks feeding on ground-dwelling birds (for immature stages) and mammals (for adult stages) in Brazil16, Argentina17, and the United States15,17,18. However, currently, we know little about these new American Borrelia strains: Only a small DNA fragment of the flagellin flaB gene has been used as an exclusive marker for their identification15–18. Unfortunately, this short gene fragment is inadequate for inferring their phylogenetic proximity with known Borrelia species since the inner tree topology remains poorly resolved at many nodes because of insufficient sequence polymorphism15–18.
In this study, we describe a novel species, belonging to the third Borrelia group, in passerine-associated ticks from tropical rainforests of French Guiana. This remote territory is a vast equatorial land located on the north-east coast of South America, mostly covered by dense rainforests and with a low density of human population. This novel Borrelia species is common in two tick species feeding on a variety of mammal and bird species. We further cultivated this bacterium and sequenced its complete genome, which showed that this novel Borrelia is intermediate between LD and RF Borrelia, sharing common features with both of them.
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Results
A novel Borrelia species in passerine-associated ticks
A total of 290 tick specimens were collected from 16 sites in French Guiana (from 2012 to 2018), mostly located along the coastline (Table S1 and Fig. 1). Most of the specimens were larvae (n = 274), with only few nymphs (n = 16), and no adults (Table S1). The 290 ticks were collected from 26 bird species, mainly the blue-backed manakin, Chiroxiphia pareola (n = 98 ticks; 34%), the wedge-billed woodcreeper, Glyphorynchus spirurus (n = 75; 26%), and the crimson-hooded manakin, Pipra aureola (n = 33; 11%). Morphological and genetic examination of tick specimens led to the identification of six tick species, all belonging to the Amblyomma genus: A. longirostre (n = 230), A. geayi (n = 52), A. varium (n = 4), A. cajennense (n = 2), A. calcaratum (n = 1), and A. humerale (n = 1). A. longirostre was found in 25 bird species, A. geayi in 11, and the four other Amblyomma species in one or two bird species each (Table S1 and Fig. 2).
More at this link: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7327063/
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