Quantitative analysis of Anaplasma marginale acquisition and transmission by Dermacentor andersoni fed in vitro

Rubikah Vimonish,Wendell C Johnson,Massaro W Ueti,Susan M Noh,Kelly A Brayton,Michelle R Mousel,Glen A Scoles

doi:10.1038/s41598-019-57390-y

Rubikah Vimonish, Wendell C Johnson + Show 5 more

Open Access

https://doi.org/10.1038/s41598-019-57390-y

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Abstract

In this study, we describe a new in vitro tick feeding system that facilitates the study of ticks and tick-borne pathogens. To optimize the system, we used Dermacentor andersoni and Anaplasma marginale as a tick-pathogen interaction model. Ticks were fed on bovine blood containing 10-fold dilutions of the pathogen to determine the effect of dose on tick infection rate. After feeding on infected blood, ticks were transferred to uninfected blood to stimulate bacterial replication within the tick vector. During stimulation feeding, blood samples were collected daily to determine if infected ticks secreted viable A. marginale. The results demonstrated similar attachment rates between the first and second tick feeding. Tick midgut and salivary glands were infected with A. marginale. However, salivary gland infection rates decreased as the percentage of parasitized erythrocytes decreased during tick acquisition feeding. Bacteria recovered from the in vitro system were able to infect a naïve bovine host. Using the highly transmissible A. marginale St. Maries strain, we demonstrated that the artificial tick feeding system is a suitable tool to study tick-pathogen interactions and that A. marginale tick salivary gland infection is dose dependent. This work demonstrates the utility of an artificial tick feeding system to directly study the association between the number of acquired pathogens and transmissibility by ticks.

Highlights

In this study, we describe a new in vitro tick feeding system that facilitates the study of ticks and tickborne pathogens
Such studies require the use of an infected mammal to rear infected ticks[13,14], limiting our ability to tightly control the delivery of the pathogen and accompanying blood meal to the tick vectors
In this study, using the in vitro tick feeding system, we first determined if A. marginale could successfully complete its life cycle within D. andersoni by demonstrating tick midgut and salivary gland infection and the secretion of viable organisms from the tick salivary glands during the transmission feed

Summary

Introduction

We describe a new in vitro tick feeding system that facilitates the study of ticks and tickborne pathogens. Understanding the key events at the tick-pathogen interface is the foundation for developing strategies to control tick-borne diseases Such studies require the use of an infected mammal to rear infected ticks[13,14], limiting our ability to tightly control the delivery of the pathogen and accompanying blood meal to the tick vectors. To address this limitation, we have developed a novel in vitro tick feeding system. In this study, using the in vitro tick feeding system, we first determined if A. marginale could successfully complete its life cycle within D. andersoni by demonstrating tick midgut and salivary gland infection and the secretion of viable organisms from the tick salivary glands during the transmission feed. Four A. marginale doses were delivered concurrently to four different groups of ticks in order to determine the effect of dose on tick infection rates and the number of bacteria in tick midgut and salivary glands

Methods

Results

Conclusion