Dataset Information

Motor rotation is essential for the formation of the periplasmic flagellar ribbon, cellular morphology, and Borrelia burgdorferi persistence within Ixodes scapularis tick and murine hosts.

ABSTRACT: Borrelia burgdorferi must migrate within and between its arthropod and mammalian hosts in order to complete its natural enzootic cycle. During tick feeding, the spirochete transmits from the tick to the host dermis, eventually colonizing and persisting within multiple, distant tissues. This dissemination modality suggests that flagellar motor rotation and, by extension, motility are crucial for infection. We recently reported that a nonmotile flaB mutant that lacks periplasmic flagella is rod shaped and unable to infect mice by needle or tick bite. However, those studies could not differentiate whether motor rotation or merely the possession of the periplasmic flagella was crucial for cellular morphology and host persistence. Here, we constructed and characterized a motB mutant that is nonmotile but retains its periplasmic flagella. Even though ?motB bacteria assembled flagella, part of the mutant cell is rod shaped. Cryoelectron tomography revealed that the flagellar ribbons are distorted in the mutant cells, indicating that motor rotation is essential for spirochetal flat-wave morphology. The ?motB cells are unable to infect mice, survive in the vector, or migrate out of the tick. Coinfection studies determined that the presence of these nonmotile ?motB cells has no effect on the clearance of wild-type spirochetes during murine infection and vice versa. Together, our data demonstrate that while flagellar motor rotation is necessary for spirochetal morphology and motility, the periplasmic flagella display no additional properties related to immune clearance and persistence within relevant hosts.

SUBMITTER: Sultan SZ

PROVIDER: S-EPMC4399055 | biostudies-literature | 2015 May

REPOSITORIES: biostudies-literature

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Motor rotation is essential for the formation of the periplasmic flagellar ribbon, cellular morphology, and Borrelia burgdorferi persistence within Ixodes scapularis tick and murine hosts.

Sultan Syed Z SZ Sekar Padmapriya P Zhao Xiaowei X Manne Akarsh A Liu Jun J Wooten R Mark RM Motaleb M A MA

Infection and immunity 20150217 5

Borrelia burgdorferi must migrate within and between its arthropod and mammalian hosts in order to complete its natural enzootic cycle. During tick feeding, the spirochete transmits from the tick to the host dermis, eventually colonizing and persisting within multiple, distant tissues. This dissemination modality suggests that flagellar motor rotation and, by extension, motility are crucial for infection. We recently reported that a nonmotile flaB mutant that lacks periplasmic flagella is rod sh ...[more]

PMID: 25690096

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Project description:BackgroundLyme disease (LD) caused by Borrelia burgdorferi is the most prevalent tick-borne disease. There is evidence that vaccines based on tick proteins that promote tick transmission of B. burgdorferi could prevent LD. As Ixodes scapularis nymph tick bites are responsible for most LD cases, this study sought to identify nymph tick saliva proteins associated with B. burgdorferi transmission using LC-MS/MS. Tick saliva was collected using a non-invasive method of stimulating ticks (uninfected and infected: unfed, and every 12 h during feeding through 72 h, and fully-fed) to salivate into 2% pilocarpine-PBS for protein identification using LC-MS/MS.ResultsWe identified a combined 747 tick saliva proteins of uninfected and B. burgdorferi infected ticks that were classified into 25 functional categories: housekeeping-like (48%), unknown function (18%), protease inhibitors (9%), immune-related (6%), proteases (8%), extracellular matrix (7%), and small categories that account for <5% each. Notably, B. burgdorferi infected ticks secreted high number of saliva proteins (n=645) than uninfected ticks (n=376). Counter-intuitively, antimicrobial peptides, which function to block bacterial infection at tick feeding site were suppressed 23-85 folds in B. burgdorferi infected ticks. Similar to glycolysis enzymes being enhanced in mammalian cells exposed to B. burgdorferi : eight of the 10-glycolysis pathway enzymes were secreted at high abundance by B. burgdorferi infected ticks. Of significance, rabbits exposed to B. burgdorferi infected ticks acquired potent immunity that caused 40-60% mortality of B. burgdorferi infected ticks during the second infestation compared to 15-28% for the uninfected. This might be explained by ELISA data that show that high expression levels of immunogenic proteins in B. burgdorferi infected ticks.ConclusionData here suggest that B. burgdorferi infection modified protein content in tick saliva to promote its survival at the tick feeding site. For instance, enzymes; copper/zinc superoxide dismutase that led to production of H2O2 that is toxic to B. burgdorferi were suppressed, while, catalase and thioredoxin that neutralize H2O2, and pyruvate kinase which yields pyruvate that protects Bb from H2O2 killing were enhanced. We conclude data here is an important resource for discovery of effective antigens for a vaccine to prevent LD.

Project description:The blacklegged tick, Ixodes scapularis, is established in several regions of Ontario, Canada, and continues to spread into new geographic areas across the province at a rapid rate. This poses a significant public health risk since I. scapularis transmits the Lyme disease-causing bacterium, Borrelia burgdorferi, and other pathogens of potential public health concern. The objective of this study was to develop species distribution models for I. scapularis and B. burgdorferi to predict and compare the potential distributions of the tick vector and the Lyme disease pathogen as well as the ecological factors most important for species establishment. Ticks were collected via tick dragging at 120 sites across southern, central, and eastern Ontario between 2015 and 2018 and tested for tick-borne pathogens. A maximum entropy (Maxent) approach was used to model the potential distributions of I. scapularis and B. burgdorferi. Two independent datasets derived from tick dragging at 25 new sites in 2019 and ticks submitted by the public to local health units between 2015 and 2017 were used to validate the predictive accuracy of the models. The model for I. scapularis showed high suitability for blacklegged ticks in eastern Ontario and some regions along the shorelines of the Great Lakes, and moderate suitability near Algonquin Provincial Park and the Georgian Bay with good predictive accuracy (tick dragging 2019: AUC = 0.898; ticks from public: AUC = 0.727). The model for B. burgdorferi showed a similar predicted distribution but was more constrained to eastern Ontario, particularly between Ottawa and Kingston, and along Lake Ontario, with similarly good predictive accuracy (tick dragging 2019: AUC = 0.958; ticks from public: AUC = 0.863. The ecological variables most important for predicting the distributions of I. scapularis and B. burgdorferi included elevation, distance to deciduous and coniferous forest, proportions of agricultural land, water, and infrastructure, mean summer/spring temperature, and cumulative annual degree days above 0°C. Our study presents a novel application of species distribution modelling for I. scapularis and B. burgdorferi in Ontario, Canada, and provides an up to date projection of their potential distributions for public health knowledge users.

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Dataset Information

Motor rotation is essential for the formation of the periplasmic flagellar ribbon, cellular morphology, and Borrelia burgdorferi persistence within Ixodes scapularis tick and murine hosts.

Publications

Motor rotation is essential for the formation of the periplasmic flagellar ribbon, cellular morphology, and Borrelia burgdorferi persistence within Ixodes scapularis tick and murine hosts.

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