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Transmission Dynamics of Borrelia turicatae from the Arthropod Vector

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      Abstract

      Background

      With the global distribution, morbidity, and mortality associated with tick and louse-borne relapsing fever spirochetes, it is important to understand the dynamics of vector colonization by the bacteria and transmission to the host. Tick-borne relapsing fever spirochetes are blood-borne pathogens transmitted through the saliva of soft ticks, yet little is known about the transmission capability of these pathogens during the relatively short bloodmeal. This study was therefore initiated to understand the transmission dynamics of the relapsing fever spirochete Borrelia turicatae from the vector Ornithodoros turicata, and the subsequent dissemination of the bacteria upon entry into murine blood.

      Methodology/Principal Findings

      To determine the minimum number of ticks required to transmit spirochetes, one to three infected O. turicata were allowed to feed to repletion on individual mice. Murine infection and dissemination of the spirochetes was evaluated by dark field microscopy of blood, quantitative PCR, and immunoblotting against B. turicatae protein lysates and a recombinant antigen, the Borrelia immunogenic protein A. Transmission frequencies were also determined by interrupting the bloodmeal 15 seconds after tick attachment. Scanning electron microscopy (SEM) was performed on infected salivary glands to detect spirochetes within acini lumen and excretory ducts. Furthermore, spirochete colonization and dissemination from the bite site was investigated by feeding infected O. turicata on the ears of mice, removing the attachment site after engorment, and evaluating murine infection.

      Conclusion/Significance

      Our findings demonstrated that three ticks provided a sufficient infectious dose to infect nearly all animals, and B. turicatae was transmitted within seconds of tick attachment. Spirochetes were also detected in acini lumen of salivary glands by SEM. Upon host entry, B. turicatae did not require colonization of the bite site to establish murine infection. These results suggest that once B. turicatae colonizes the salivary glands the spirochetes are preadapted for rapid entry into the mammal.

      Author Summary

      Relapsing fever spirochetes cause recurrent febrile episodes, rigors, nausea, vomiting, malaise, and pregnancy complications, and are a leading cause of hospital admissions in regions of Africa. Routes of pathogen transmission include crushed human body lice and feces, or through bites by Ornithodoros spp. of ticks. The life cycle of Ornithodoros turicatae, the vector of Borrelia turicatae, includes over six nymphal stages, upwards of a ten year life span, and a bloodmeal that is completed within an hour. We investigated B. turicatae transmission from the tick vector and assessed the rapidity of spirochete entry into the mammal and dissemination in the blood. Salivary glands from infected ticks were also evaluated to visualize B. turicatae within the tissues to determine spirochete localization. We conclude that given the transmission dynamics of B. turicatae, it may be important to target conserved surface proteins that relapsing fever spirochetes produce in the salivary glands in order to develop preventative measures against the pathogens.

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      Most cited references 30

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      Isolation and cultivation of Lyme disease spirochetes.

       A Barbour (1984)
      The successful isolation and cultivation of Lyme disease spirochetes traces its lineage to early attempts at cultivating relapsing fever borreliae. Observations on the growth of Lyme disease spirochetes under different in vitro conditions may yield important clues to both the metabolic characteristics of these newly discovered organisms and the pathogenesis of Lyme disease. Images FIG. 1
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        The Lyme disease agent exploits a tick protein to infect the mammalian host.

        The Lyme disease agent, Borrelia burgdorferi, is maintained in a tick-mouse cycle. Here we show that B. burgdorferi usurps a tick salivary protein, Salp15 (ref. 3), to facilitate the infection of mice. The level of salp15 expression was selectively enhanced by the presence of B. burgdorferi in Ixodes scapularis, first indicating that spirochaetes might use Salp15 during transmission. Salp15 was then shown to adhere to the spirochaete, both in vitro and in vivo, and specifically interacted with B. burgdorferi outer surface protein C. The binding of Salp15 protected B. burgdorferi from antibody-mediated killing in vitro and provided spirochaetes with a marked advantage when they were inoculated into naive mice or animals previously infected with B. burgdorferi. Moreover, RNA interference-mediated repression of salp15 in I. scapularis drastically reduced the capacity of tick-borne spirochaetes to infect mice. These results show the capacity of a pathogen to use a secreted arthropod protein to help it colonize the mammalian host.
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          TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi.

          The Lyme disease agent Borrelia burgdorferi naturally persists in a cycle that primarily involves ticks and mammals. We have now identified a tick receptor (TROSPA) that is required for spirochetal colonization of Ixodes scapularis. B. burgdorferi outer surface protein A, which is abundantly expressed on spirochetes within the arthropod and essential for pathogen adherence to the vector, specifically bound to TROSPA. TROSPA mRNA levels in ticks increased following spirochete infestation and decreased in response to engorgement, events that are temporally linked to B. burgdorferi entry into and egress from the vector. The blockade of TROSPA by TROSPA antisera or by the repression of TROSPA expression via RNA interference reduced B. burgdorferi adherence to the I. scapularis gut in vivo, thereby preventing efficient colonization of the vector and subsequently reducing pathogen transmission to the mammalian host. Identification of an I. scapularis receptor for B. burgdorferi is the first step toward elucidating arthropod ligands that are required for survival of spirochetes in nature.
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            Author and article information

            Affiliations
            [1 ]Department of Biological Sciences, Mississippi State University, Starkville, Mississippi, United States of America
            [2 ]Institute for Imaging and Analytical Technologies, Mississippi State University, Starkville, Mississippi, United States of America
            University of California San Diego School of Medicine, United States of America
            Author notes

            The authors have declared that no competing interest exist.

            Conceived and designed the experiments: WKB JEL. Performed the experiments: WKB HKW AML JEL. Analyzed the data: WKB JEL. Contributed reagents/materials/analysis tools: AML JEL. Wrote the paper: WKB JEL.

            Contributors
            Role: Editor
            Journal
            PLoS Negl Trop Dis
            PLoS Negl Trop Dis
            plos
            plosntds
            PLoS Neglected Tropical Diseases
            Public Library of Science (San Francisco, USA )
            1935-2727
            1935-2735
            April 2014
            3 April 2014
            : 8
            : 4
            24699275 3974661 PNTD-D-13-01945 10.1371/journal.pntd.0002767

            This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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            Pages: 8
            Funding
            Start up funds provided by Mississippi State University, 1K22AI091652-01A1, 1R21AI103724-01A1. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
            Categories
            Research Article
            Medicine and Health Sciences
            Infectious Diseases
            Bacterial Diseases
            Borrelia Infection
            Tropical Diseases
            Neglected Tropical Diseases

            Infectious disease & Microbiology

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