Tick–Pathogen Interactions: The Metabolic Perspective

Abstract

The first tick genome published in 2016 provided an invaluable tool for studying the molecular basis of tick-pathogen interactions. Metabolism is a key element in host-pathogen interactions. However, our knowledge of tick-pathogen metabolic interactions is very limited. Recently, a systems biology approach, using omics datasets, has revealed that tick-borne pathogen infection induces transcriptional reprograming affecting several metabolic pathways in ticks, facilitating infection, multiplication, and transmission. Results suggest that the response of tick cells to tick-borne pathogens is associated with tolerance to infection. Here we review our current understanding of the modulation of tick metabolism by tick-borne pathogens, with a focus on the model intracellular bacterium Anaplasma phagocytophilum. Tick-Pathogen Metabolic Interactions at the Center of the Infectious Storm Metabolism is key to cellular function [1,2]. In consequence, all major molecular pathways in living cells are interconnected to, and regulated by, the availability and levels of metabolites [1,2]. Recent studies in mammalian cells showed that interactions between intracellular bacterial pathogens and the host cells can lead to physiological changes in both interacting members [3]. The metabolic adaptations in mammalian cell-pathogen systems promote proliferation or elimination of the pathogen within the host cells [3]. Tick-pathogen interactions, however, involve a more complex array of outcomes which include conflict and cooperation that ultimately benefit both ticks and pathogens [4]. This is not surprising considering that, in vector-borne pathogen systems, the survival of the vector is essential for the completion of the life cycle of the pathogen. In addition, tick-borne pathogen infection increases tick performance in challenging environmental conditions [5,6]. Therefore, in some cases, vector tolerance to pathogen infection is an advantageous life trait in arthropod vectors [7]. Modulation of tick metabolism by tick-borne pathogens is a result of coevolution and adaption to a considerable number of tick and reservoir host species [4,8,9]. The Ixodes scapularis genome, the first for a medically important chelicerate, is the only tick genome available so far [10]. The sequencing of the I. scapularis genome was an essential step towards the understanding of the molecular processes that support the parasitic lifestyle of the tick and its success as a vector of multiple pathogens, including bacteria, viruses, protozoa, and helminths, which constitute a growing burden for human and animal health worldwide [11]. This review focuses on recent research that provided insights on the finely tuned metabolic changes that the model pathogen A. phagocytophilum induces in its tick vector I. scapularis. For comparative purposes, tick metabolic changes induced by other pathogens, including mainly Borrelia spp., flaviviruses, and fungi, will be also included (Table 1). Results suggest that tickborne pathogens use tick metabolism as a hub to modulate ...

Vector competence of the African argasid tick Ornithodoros moubata for the Q fever agent Coxiella burnetii

“…The fact that ticks and not G. mellonella are tolerant to C. burnetii may highlight pivotal biological differences between these arthropods. Indeed, recent observations showed that intracellular tick-borne pathogens modulate tick physiology and tick cell processes, including immunity and apoptosis, leading to tolerance of intracellular infections [41]. A similar modulation of O. moubata metabolism by C. burnetii may thus take place, not impacting tick survival and subsequently enhancing their vector competence.…”

Interactions Between Ticks and Lyme Disease Spirochetes

“…Using gas chromatography coupled to a mass spectrometry-based approach, a recent study explored the differences between the metabolic profiles of B. burgdorferi-infected and naïve I. scapularis nymphal ticks during blood meal engorgement (Hoxmeier et al, 2017). Additional studies on tick-pathogen metabolic interactions (see review (Cabezas-Cruz et al, 2019)) are certainly warranted, as they will contribute both to our understanding of the complex interactions between B. burgdorferi and Ixodes ticks, and to the development of novel interventions against tick-borne infections.…”

Comparative Proteomic Analysis of Rhipicephalus sanguineus sensu lato (Acari: Ixodidae) Tropical and Temperate Lineages: Uncovering Differences During Ehrlichia canis Infection

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