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

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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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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Cholinergic axons regulate type I acini in salivary glands of Ixodes ricinus and Ixodes scapularis ticks

Scientific Reports ◽

10.1038/s41598-020-73077-1 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Lourdes Mateos-Hernandéz ◽

Baptiste Defaye ◽

Marie Vancová ◽

Ondrej Hajdusek ◽

Radek Sima ◽

...

Keyword(s):

Salivary Glands ◽

Signaling Pathway ◽

Water Uptake ◽

Receptor Activation ◽

Muscarinic Acetylcholine Receptors ◽

Water Volume ◽

Neural Cells ◽

Type I ◽

Hard Tick

Abstract Regulatory factors controlling tick salivary glands (SGs) are direct upstream neural signaling pathways arising from the tick’s central nervous system. Here we investigated the cholinergic signaling pathway in the SG of two hard tick species. We reconstructed the organization of the cholinergic gene locus, and then used in situ hybridization to localize mRNA encoding choline acetyltransferase (ChAT) and vesicular acetylcholine transporter (VAChT) in specific neural cells in the Ixodes synganglion. Immunohistochemical staining revealed that cholinergic axonal projections exclusively reached type I acini in the SG of both Ixodes species. In type I acini, the rich network of cholinergic axons terminate within the basolateral infoldings of the lamellate cells. We also characterized two types (A and B) of muscarinic acetylcholine receptors (mAChRs), which were expressed in Ixodes SG. We pharmacologically assessed mAChR-A to monitor intracellular calcium mobilization upon receptor activation. In vivo injection of vesamicol—a VAChT blocker—at the cholinergic synapse, suppressed forced water uptake by desiccated ticks, while injection of atropine, an mAChR-A antagonist, did not show any effect on water volume uptake. This study has uncovered a novel neurotransmitter signaling pathway in Ixodes SG, and suggests its role in water uptake by type I acini in desiccated ticks.

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

Infection Genetics and Evolution ◽

10.1016/j.meegid.2014.04.022 ◽

2014 ◽

Vol 27 ◽

pp. 551-558 ◽

Cited By ~ 37

Author(s):

Alan G. Barbour

Keyword(s):

Ixodes Scapularis ◽

Hard Tick ◽

Relapsing Fever

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Purification and cloning of a novel antimicrobial peptide from salivary glands of the hard tick, Ixodes sinensis

Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology ◽

10.1016/j.cbpb.2007.10.002 ◽

2008 ◽

Vol 149 (4) ◽

pp. 557-561 ◽

Cited By ~ 17

Author(s):

Zhigang Liu ◽

Huan Liu ◽

Xiaoyu Liu ◽

Xuli Wu

Keyword(s):

Antimicrobial Peptide ◽

Salivary Glands ◽

Hard Tick

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A novel antimicrobial peptide from salivary glands of the hard tick, Ixodes sinensis

Peptides ◽

10.1016/j.peptides.2005.06.020 ◽

2006 ◽

Vol 27 (1) ◽

pp. 31-35 ◽

Cited By ~ 33

Author(s):

Da Yu ◽

Zonggen Sheng ◽

Xueqing Xu ◽

Jianxu Li ◽

Hailong Yang ◽

...

Keyword(s):

Antimicrobial Peptide ◽

Salivary Glands ◽

Hard Tick

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Vector Competence of Geographical Populations ofOrnithodoros turicatafor the Tick-Borne Relapsing Fever SpirocheteBorrelia turicatae

Applied and Environmental Microbiology ◽

10.1128/aem.01505-18 ◽

2018 ◽

Vol 84 (21) ◽

Cited By ~ 5

Author(s):

Aparna Krishnavajhala ◽

Brittany A. Armstrong ◽

Job E. Lopez

Keyword(s):

Salivary Glands ◽

Vector Competence ◽

Relapsing Fever ◽

Tick Saliva ◽

Eastern Population ◽

Content Type ◽

Western Population ◽

Geographical Populations ◽

Globally Distributed ◽

Two Populations

ABSTRACTVector competence refers to the ability of an arthropod to acquire, maintain, and successfully transmit a microbial pathogen. Tick-borne relapsing fever (TBRF) spirochetes are globally distributed pathogens, and most species are transmitted by argasid ticks of the genusOrnithodoros.A defining characteristic in vector competence is an apparent specificity of a species of TBRF spirochete to a given tick species. In arid regions of the southern United States,Borrelia turicataeis the primary cause of TBRF. Interestingly, there are two populations of the tick vector distributed throughout this region.Ornithodoros turicatais a western population that ranges from California to Texas. There is a gap through Louisiana, Mississippi, and Alabama where the tick has not been identified. An isolated eastern population exists in Florida and was designated a subspecies,O. turicata americanus.A knowledge gap that exists is the poor understanding of vector competence between western and eastern populations of ticks forB. turicatae.In this study, we generated uninfected colonies ofO. turicatathat originated in Texas and Kansas and ofO. turicataamericanus. B. turicataeacquisition, maintenance through the molt, and subsequent transmission were evaluated. Our findings revealed significant differences in murine infection after feeding infectedO. turicataandO. turicataamericanusticks on the animals. Interestingly, the salivary glands of both tick populations were colonized withB. turicataeto similar densities. Our results suggest that the salivary glands of the tick colonies assessed in this study impact vector competence of the evaluatedB. turicataeisolates.IMPORTANCESeveral knowledge gaps exist in the vector competence of various geographical populations ofO. turicatathat transmitB. turicatae. A western population of this tick is distributed from California to Texas, and an eastern population exists in Florida. Utilizing western and eastern populations of the vector, we studied acquisition and transmission of twoB. turicataeisolates. Regardless of the isolate used, infection frequencies were poor in mice after the eastern population feeding on them. Since salivary gland colonization is essential forB. turicataetransmission, these tissues were further evaluated. Interestingly, the salivary glands from the two populations were similarly colonized withB. turicatae.These findings suggest the role of tick saliva in the establishment of infection and that the salivary glands may be a bottleneck for successful transmission.

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