Comparative genomics of the Western Hemisphere soft tick-borne relapsing fever borreliae highlights extensive plasmid diversity

Kneubehl, Alexander R.; Krishnavajhala, Aparna; Leal, Sebastián Muñoz; Replogle, Adam J.; Kingry, Luke C.; Bermúdez, Sergio; Labruna, Marcelo B.; López, Job E.

doi:10.1186/s12864-022-08523-7

Cited by 21 publications

(51 citation statements)

References 129 publications

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“…The ML reconstruction is congruent with previous reported phylogenetic inferences [37,40,52,80,83]. In particular, the Borrelia sequences recorded from bats in the present study are closely related to genospecies isolated from Carollia perspicillata in the Department of Santander, Colombia [40].…”

Section: Discussionsupporting

confidence: 91%

Is Borrelia burgdorferi Sensu Stricto in South America? First Molecular Evidence of Its Presence in Colombia

et al. 2022

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The genus Borrelia encompasses spirochetal species that are part of three well-defined groups. Two of these groups contain pathogens that affect humans: the group causing Lyme disease (LDG) and the relapsing fever group (RFG). Lyme disease is caused by Borrelia burgdorferi s.l., which is distributed in the Northern Hemisphere, and relapsing fevers are caused by Borrelia spp., which are found in temperate and tropical countries and are an emerging but neglected pathogens. In some departments of Colombia, there are records of the presence of Borrelia sp. in humans and bats. However, little is known about the impact and circulation of Borrelia spp. in the country, especially in wildlife, which can act as a reservoir and/or amplifying host. In this context, the objective of our research was to detect and identify the Borrelia species present in wild mammals in the departments of Caldas and Risaralda in Colombia. For morphological detection, blood smears and organ imprints were performed, and molecular identification was carried out through a nested PCR directed on the flagellin B (flaB) gene. A total of 105 mammals belonging to three orders (Chiroptera, Didelphimorphia and Rodentia) were analyzed, of which 15.24% (n = 16) were positive for Borrelia. Molecularly, the presence of Borrelia burgdorferi s.s. in lung tissues of Thomasomys aureus and blood of Mus musculus (Rodentia) was detected, with 99.64 and 100% identity, respectively. Borrelia sp. genospecies from a clade branch of a bat-associated LDG sister group were identified in seven individuals of bat species, such as Artibeus lituratus, Carollia brevicauda, Sturnira erythromos, and Glossophaga soricina. Furthermore, two Borrelia genospecies from the RFG in seven individuals of bats (A. lituratus, Artibeus jamaicensis, Platyrrhinus helleri, Mesophylla macconnelli, Rhynchonycteris naso) and rodents (Coendou rufescens, Microryzomys altissimus) were documented. Additionally, the presence of a spirochete was detected by microscopy in the liver of a Sturnira erythromos bat specimen. These results contain the first molecular evidence of the presence of B. burgdorferi s.s. in South America, which merits the need for comprehensive studies involving arthropods and vertebrates (including humans) in other departments of Colombia, as well as neighboring countries, to understand the current status of the circulation of Borrelia spp. in South America.

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Section: Discussionsupporting

confidence: 91%

Is Borrelia burgdorferi Sensu Stricto in South America? First Molecular Evidence of Its Presence in Colombia

et al. 2022

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“…During this century, Muñoz-Leal et al [ 13 ] isolated B. venezuelensis by feeding Ornithodoros rudis from Maranhão state on Vesper mice ( Calomys callosus ). Subsequently, this isolate (designated as B. venezuelensis RMA01) was cultured in vitro and its genome sequenced [ 14 ]. Borrelia venezuelensis RMA01 constitutes to date the sole isolate of a RFG borreliae transmitted by an Ornithodoros tick in South America [ 11 ].…”

Section: Introductionmentioning

confidence: 99%

A Novel Relapsing Fever Group Borrelia Isolated from Ornithodoros Ticks of the Brazilian Caatinga

et al. 2023

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Tick-borne relapsing fever group (RFG) borreliosis remains neglected as a human disease and little is known on its maintenance in ticks and vertebrates, especially in South America. Therefore, this study investigated borrelial infection in Ornithodoros ticks collected in rodent-inhabited rock formations in the Brazilian semiarid region, within the Caatinga biome. Collected ticks (Ornithodoros rietcorreai and Ornithodoros cf. tabajara) were allowed to feed under laboratory conditions on guinea pigs, which had blood samples examined daily by dark-field microscopy. No spirochetes were visualized in the blood of any of four O. rietcorreai-infested guinea pigs. Contrastingly, spirochetes were visualized between 9 and 39 days after tick feeding in the blood of three guinea pigs, each infested with O. cf. tabajara ticks from a different locality. Guinea pig infection was confirmed by passages into experimental animals and by generating DNA sequences of Borrelia spp. from the blood of spirochetemic guinea pigs. Three O. cf. tabajara populations were infected by the same borrelial organism, which was characterized as a novel RFG agent (named as ‘Candidatus Borrelia caatinga’) based on 10 Borrelia loci (rrs, flaB, glpQ, gyrB, clpX, pepX, pyrG, recG, rplB and uvrA). We demonstrated that O. cf. tabajara is a competent vector of the novel Borrelia sp. isolates, although none of the infected rodents developed clinical illness.

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“…Within the WHsTBRF spirochetes, BLASTp found similar proteins (∼40% sequence similarity, 99% query coverage, e-value= 0.0) in B. puertoricensis SUM (bpuSUM_001813, linear plasmid 46 ‘lp46’), B. parkeri SLO (bpSLO_001255, lp28), and in B. venezuelensis RMA01 (bvRMA01_001103, lp25). Interestingly, these plasmids are not in the same plasmid family (1). Further, BLASTn nor BLASTp did not detect genes or proteins similar to bhDAH_001311 in B. hermsii YOR or any other B. hermsii genomic group II sequences deposited in GenBank.…”

Section: Resultsmentioning

confidence: 99%

“…The F27 plasmid family was the shortest linear plasmid family found in all WHsTBRF species (1). The size ranged between ∼10kb to ∼12kb.…”

Section: Resultsmentioning

confidence: 99%

Comparative genomics analysis of three conserved plasmid families in the Western Hemisphere soft tick-borne relapsing fever borreliae provides insight into variation in genome structure and antigenic variation systems

Kneubehl

López

2023

Preprint

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Borreliaspirochetes, causative agents of Lyme disease and relapsing fever (RF), have a uniquely complex genome consisting of a linear chromosome and circular and linear plasmids. The plasmids harbor genes important for the vector-host life cycle of these tick-borne bacteria. The role of Lyme disease causingBorreliaplasmids is more refined compared to RF spirochetes because of limited plasmid-resolved genomes for RF spirochetes. We recently addressed this limitation and found that three linear plasmid families (F6, F27, and F28) were syntenic across all species. Given this conservation, we further investigated the three plasmid families. The F6 family, also known as the megaplasmid, contained regions of repetitive DNA. The F27 was the smallest, encoding genes with unknown function. The F28 family encoded the expression locus for antigenic variation in all species exceptBorrelia hermsiiandBorrelia anserina.Taken together, this work provides a foundation for future investigations to identify essential plasmid-localized genes that drive the vector-host life cycle of RFBorrelia.IMPORTANCEBorreliaspp. spirochetes are arthropod-borne bacteria found globally and infect humans and other vertebrates. RF borreliae are understudied and misdiagnosed pathogens because of the vague clinical presentation of disease and the elusive feeding behavior of argasid ticks. Consequently, genomics resources for RF spirochetes have been limited. Analyses ofBorreliaplasmids have been challenging because they are often highly fragmented and unassembled. By utilizing Oxford Nanopore Technologies, we recently generated plasmid-resolved genomes for sevenBorreliaspp. found in the Western Hemisphere. This current study is a more in-depth investigation into the linear plasmids that were conserved and syntenic across species. This analysis determined differences in genome structure and, importantly, in antigenic variation systems between species. This work is an important step in identifying crucial plasmid-borne genetic elements essential for the life cycle of RF spirochetes.

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Comparative genomics of the Western Hemisphere soft tick-borne relapsing fever borreliae highlights extensive plasmid diversity

Cited by 21 publications

References 129 publications

Is Borrelia burgdorferi Sensu Stricto in South America? First Molecular Evidence of Its Presence in Colombia

Is Borrelia burgdorferi Sensu Stricto in South America? First Molecular Evidence of Its Presence in Colombia

A Novel Relapsing Fever Group Borrelia Isolated from Ornithodoros Ticks of the Brazilian Caatinga

Comparative genomics analysis of three conserved plasmid families in the Western Hemisphere soft tick-borne relapsing fever borreliae provides insight into variation in genome structure and antigenic variation systems

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