Phylogeny of a relapsing fever Borrelia species transmitted by the hard tick Ixodes scapularis

Abstract Background Relapsing fever (RF) borreliae are arthropod-borne spirochetes and some of them cause human diseases, which are characterized by relapsing or recurring episodes of fever. Recently, it has been classified into two groups: soft tick-borne RF (STRF) borreliae and hard tick-borne RF (HTRF) borreliae. STRF borreliae include classical RF agents and HTRF borreliae, the latter of which include B. miyamotoi, a human pathogen recently identified in Eurasia and North America. Results In this study, we determined the genome sequences of 16 HTRF borreliae strains: 15 B. miyamotoi strains (9 from Hokkaido Island, Japan, 3 from Honshu Island, Japan, and 3 from Mongolia) and a Borrelia sp. tHM16w. Chromosomal gene synteny was highly conserved among the HTRF strains sequenced in this study, even though they were isolated from different geographic regions and different tick species. Phylogenetic analysis based on core gene sequences revealed that HTRF and STRF borreliae are clearly distinguishable, with each forming a monophyletic group in the RF borreliae lineage. Moreover, the evolutionary relationships of RF borreliae are consistent with the biological and ecological features of each RF borreliae sublineage and can explain the unique characteristics of Borrelia anserina. In addition, the pairwise genetic distances between HTRF borreliae strains were well correlated with those of vector species rather than with the geographical distances between strain isolation sites. This result suggests that the genetic diversification of HTRF borreliae is attributed to the speciation of vector ticks and that this relationship might be required for efficient transmission of HTRF borreliae within vector ticks. Conclusions The results of the present study, together with those from previous investigations, support the hypothesis that the common ancestor of borreliae was transmitted by hard-bodied ticks and that only STRF borreliae switched to using soft-bodied ticks as a vector, which was followed by the emergence of Borrelia recurrentis, lice-borne RF borreliae. Our study clarifies the phylogenetic relationships between RF borreliae, and the data obtained will contribute to a better understanding of the evolutionary history of RF borreliae.

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Borreliae Part 2: Borrelia Relapsing Fever Group and Unclassified Borrelia

Biology ◽

10.3390/biology10111117 ◽

2021 ◽

Vol 10 (11) ◽

pp. 1117

Author(s):

Giusto Trevisan ◽

Marina Cinco ◽

Sara Trevisini ◽

Nicola di Meo ◽

Maurizio Ruscio ◽

...

Keyword(s):

Geographical Distribution ◽

New World ◽

Common Ancestor ◽

Etiological Agent ◽

Hard Tick ◽

Soft Tick ◽

Relapsing Fever ◽

Old World ◽

Pediculus Humanus ◽

Candidate Species

Borreliae of the relapsing fever group (RFG) are heterogenous and can be divided mainly into three groups according to vectors, namely the soft-tick-borne relapsing fever (STBRF) Borreliae, the hard-tick-borne relapsing fever (HTBRF) Borreliae, the louse-borne relapsing fever (LBRF) Borreliae, and the avian relapsing fever ones. With respect to the geographical distribution, the STBRF Borreliae are further subdivided into Old World and New World strains. Except for the Avian relapsing fever group Borreliae, which cause avian spirochetosis, all the others share infectivity in humans. They are indeed the etiological agent of both endemic and epidemic forms of relapsing fever, causing high spirochaetemia and fever. Vectors are primarily soft ticks of Ornithodoros spp. in the STBRF group; hard ticks, notably Ixodes sp., Amblyomma sp., Dermacentor sp., and Rhipicephalus sp., in the HTBRF group; and the louse pediculus humanus humanus in the TBRF one. A recent hypothesis was supported for a common ancestor of RFG Borreliae, transmitted at the beginning by hard-body ticks. Accordingly, STBRF Borreliae switched to use soft-bodied ticks as a vector, which was followed by the use of lice by Borrelia recurrentis. There are also new candidate species of Borreliae, at present unclassified, which are also described in this review.

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A novel relapsing fever Borrelia sp. infects the salivary glands of the molted hard tick, Amblyomma geoemydae

Ticks and Tick-borne Diseases ◽

10.1016/j.ttbdis.2012.06.003 ◽

2012 ◽

Vol 3 (4) ◽

pp. 259-261 ◽

Cited By ~ 19

Author(s):

Ai Takano ◽

Chieko Sugimori ◽

Hiromi Fujita ◽

Teruki Kadosaka ◽

Kyle R. Taylor ◽

...

Keyword(s):

Salivary Glands ◽

Hard Tick ◽

Relapsing Fever

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An immunocompromised mouse model to infect Ixodes scapularis ticks with the relapsing fever spirochete, Borrelia miyamotoi

Ticks and Tick-borne Diseases ◽

10.1016/j.ttbdis.2018.11.017 ◽

2019 ◽

Vol 10 (2) ◽

pp. 352-359 ◽

Cited By ~ 6

Author(s):

Geoffrey E. Lynn ◽

Nicole E. Breuner ◽

Lars Eisen ◽

Andrias Hojgaard ◽

Adam J. Replogle ◽

...

Keyword(s):

Mouse Model ◽

Ixodes Scapularis ◽

Borrelia Miyamotoi ◽

Relapsing Fever ◽

Immunocompromised Mouse

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Blood Smears Have Poor Sensitivity for ConfirmingBorrelia miyamotoiDisease

Journal of Clinical Microbiology ◽

10.1128/jcm.01468-18 ◽

2019 ◽

Vol 57 (3) ◽

Cited By ~ 1

Author(s):

Sam R. Telford ◽

Heidi K. Goethert ◽

Philip J. Molloy ◽

Victor Berardi

Keyword(s):

Lyme Disease ◽

Morphological Evidence ◽

Hard Tick ◽

Borrelia Miyamotoi ◽

Relapsing Fever ◽

Main Mode ◽

Blood Samples ◽

Content Type ◽

Blood Smears ◽

Thick Smear

ABSTRACTBorrelia miyamotoidisease (BMD) is a newly recognized borreliosis that is cotransmitted by ticks wherever Lyme disease is zoonotic. UnlikeBorrelia burgdorferisensu lato, the agent of Lyme disease,B. miyamotoiis closely related to relapsing fever spirochetes, such asBorrelia hermsii. Some authors have suggested that the disease caused byB. miyamotoishould be considered a hard-tick-transmitted relapsing fever, and thus, the main mode of confirming a diagnosis for that infection, microscopy to analyze a blood smear, may have clinical utility. To determine whether blood smears may detectB. miyamotoiin the blood of acute BMD patients, we made standard malariological thick smears from anticoagulated blood samples that were previously determined to contain this agent (by PCR) and analyzed them for morphological evidence of spirochetes. Spirochetes were not detected in the blood smears from 20 PCR positive patient blood samples after examination of 100 thick smear fields and only 2 of 20 demonstrated spirochetes when the examination was extended to 300 thick smear fields. Inoculation of severe combined immunodeficient (SCID) mice yielded isolates from 5 of 5 samples, but 0 of 3 BALB/c mice became infected. We conclude that in strong contrast to the diagnosis of typical relapsing fever, microscopy of blood smears is not sensitive enough for confirming a diagnosis of BMD but that SCID mouse inoculation could be a useful complement to PCR.

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A preliminary linkage map of the hard tick, Ixodes scapularis

Insect Molecular Biology ◽

10.1046/j.1365-2583.2003.00402.x ◽

2003 ◽

Vol 12 (2) ◽

pp. 201-210 ◽

Cited By ~ 12

Author(s):

A. J. Ullmann ◽

J. Piesman ◽

M. C. Dolan ◽

W. C. Black IV

Keyword(s):

Linkage Map ◽

Ixodes Scapularis ◽

Hard Tick

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Transmission of the relapsing fever spirochete, Borrelia miyamotoi, by single transovarially-infected larval Ixodes scapularis ticks

Ticks and Tick-borne Diseases ◽

10.1016/j.ttbdis.2018.07.006 ◽

2018 ◽

Vol 9 (6) ◽

pp. 1464-1467 ◽

Cited By ~ 6

Author(s):

Nicole E. Breuner ◽

Andrias Hojgaard ◽

Adam J. Replogle ◽

Karen A. Boegler ◽

Lars Eisen

Keyword(s):

Ixodes Scapularis ◽

Borrelia Miyamotoi ◽

Relapsing Fever

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In Vitro Susceptibility of the Relapsing-Fever Spirochete Borrelia miyamotoi to Antimicrobial Agents

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.00535-17 ◽

2017 ◽

Vol 61 (9) ◽

Cited By ~ 9

Author(s):

Joris Koetsveld ◽

Ronald O. P. Draga ◽

Alex Wagemakers ◽

Annemijn Manger ◽

Anneke Oei ◽

...

Keyword(s):

Antimicrobial Agents ◽

Minimal Bactericidal Concentration ◽

Hard Tick ◽

Borrelia Miyamotoi ◽

Relapsing Fever ◽

In Vitro Susceptibility ◽

Content Type ◽

Microtiter Plates ◽

Microdilution Method

ABSTRACT Hard-tick-borne relapsing fever (HTBRF) is an emerging infectious disease throughout the temperate zone caused by the relapsing-fever spirochete Borrelia miyamotoi. Antibiotic treatment of HTBRF is empirically based on the treatment of Lyme borreliosis; however, the antibiotic susceptibility of B. miyamotoi has not been studied to date. Thus, we set out to determine the in vitro antimicrobial susceptibility of B. miyamotoi. A microdilution method with 96-well microtiter plates was used to determine the antibiotic susceptibilities of two B. miyamotoi strains isolated on two different continents (Asia and North America), two Borrelia burgdorferi sensu lato strains, and one Borrelia hermsii isolate for purposes of comparison. The MIC and minimal bactericidal concentration (MBC) were determined by both microscopy and colorimetric assays. We were able to show that relative to the B. burgdorferi sensu lato isolates, both B. miyamotoi strains and B. hermsii demonstrated greater susceptibility to doxycycline and azithromycin, equal susceptibility to ceftriaxone, and resistance to amoxicillin in vitro. The MIC and MBC of amoxicillin for B. miyamotoi evaluated by microscopy were 16 to 32 mg/liter and 32 to 128 mg/liter, respectively. Since B. miyamotoi is susceptible to doxycycline, azithromycin, and ceftriaxone in vitro, our data suggest that these antibiotics can be used for the treatment of HTBRF. Oral amoxicillin is currently used as an alternative for the treatment of HTBRF; however, since we found that the B. miyamotoi strains tested were resistant to amoxicillin in vitro, this issue warrants further study.

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