Grappling with the tick microbiome

Narasimhan, Sukanya; Swei, Andrea; Abouneameh, Selma; Pal, Utpal; Pedra, Joao H. F.; Fikrig, Erol

doi:10.1016/j.pt.2021.04.004

Cited by 65 publications

(61 citation statements)

References 108 publications

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“…Most tick species typically harbor a single lineage of nutritional symbiont, but multiple symbiont lineages exist in different tick species ( Duron and Gottlieb, 2020 ). The most common lineages belong to the Coxiella -like endosymbiont group and to the Francisella -like endosymbiont group (CLE and FLE, hereafter) ( Azagi et al, 2017 ; Binetruy et al, 2020 ; Duron et al, 2017 ; Machado-Ferreira et al, 2016 ), but a few tick species may rely on other symbionts ( Duron et al, 2017 ), such as the Rickettsia -like endosymbionts ( Narasimhan et al, 2021 ) and the intramitochondrial bacterium Midichloria ( Sassera et al, 2006 ). Once deprived of their nutritional symbionts, ticks show a complete stop of growth and moulting, as well as lethal physical abnormalities ( Ben-Yosef et al, 2020 ; Duron et al, 2018 ; Guizzo et al, 2017 ; Zhong et al, 2007 ), which can be fully restored with an artificial supplement of B vitamins ( Duron et al, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum

Buysse

Floriano

Gottlieb

et al. 2021

eLife

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Many animals are dependent on microbial partners that provide essential nutrients lacking from their diet. Ticks, whose diet consists exclusively on vertebrate blood, rely on maternally inherited bacterial symbionts to supply B vitamins. While previously studied tick species consistently harbor a single lineage of those nutritional symbionts, we evidence here that the invasive tick Hyalomma marginatum harbors a unique dual-partner nutritional system between an ancestral symbiont, Francisella, and a more recently acquired symbiont, Midichloria. Using metagenomics, we show that Francisella exhibits extensive genome erosion that endangers the nutritional symbiotic interactions. Its genome includes folate and riboflavin biosynthesis pathways but deprived functional biotin biosynthesis on account of massive pseudogenization. Co-symbiosis compensates this deficiency since the Midichloria genome encompasses an intact biotin operon, which was primarily acquired via lateral gene transfer from unrelated intracellular bacteria commonly infecting arthropods. Thus, in H. marginatum, a mosaic of co-evolved symbionts incorporating gene combinations of distant phylogenetic origins emerged to prevent the collapse of an ancestral nutritional symbiosis. Such dual endosymbiosis was never reported in other blood feeders but was recently documented in agricultural pests feeding on plant sap, suggesting that it may be a key mechanism for advanced adaptation of arthropods to specialized diets.

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Section: Introductionmentioning

confidence: 99%

A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum

Buysse

Floriano

Gottlieb

et al. 2021

eLife

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“…The use of broad spectrum antimicrobial compounds, such as antibiotics, targeting several bacterial species does not allow establishing causal links between the reduction of specific taxa abundance in tick microbiota and changes in tick physiology or pathogen colonization. The lack of tools for the precise manipulation of the tick microbiome is currently a major limitation to achieve mechanistic insights into the tick microbiome (Narasimhan et al 2021).…”

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confidence: 99%

Anti-tick microbiota vaccines: how can this actually work?

et al. 2021

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The main importance of ticks resides in their ability to harbor and transmit microorganisms that cause disease to animals and humans. In addition to pathogens, ticks coexist and interact with symbionts, and commensal bacteria that together form an ecological unit, the tick holobiont. The holobiont is an additional organismal level on which natural selection operates. The components of the tick hologenome, composed of host and microbiome genomes, are complimentary. In agreement with this proposition, antibiotic treatment produces disturbance of the tick-microbiota homeostasis which in turn decreases tick fitness and affects tick-pathogen interactions. Accordingly, we hypothesized that immune targeting of key members of the bacterial community of the tick microbiome by host antibodies could cause microbial dysbiosis with consequences for tick physiology and vector competence. Anti-tick microbiota vaccines were recently introduced as a tool to target the microbiota of vector arthropods by immunizing the vertebrate hosts against live keystone bacteria or tick microbiota bacterial proteins. This tool can also be used to target tick endosymbionts. Decreased abundance of selected keystone bacteria and/or endosymbionts may reshape the structure of tick microbial communities in a predictable manner. This tool can be used to manipulate the tick microbiome against ticks and transmitted pathogens. In this opinion, we explore the possibilities of this methodology for the control of ticks and tick-borne diseases.

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“…Whether this is through microbial-mediated immune evasion/suppression or through immunological tolerance from the arthropod is not clearly defined ( Sonenshine and Macaluso, 2017 ; Shaw et al, 2018 ; Boulanger and Wikel, 2021 ; Rosche et al, 2021 ). Prolonged nutrient limitation between bloodmeals and competition with the resident microbiota/endogenous virome are also restrictive forces that must be dealt with ( Bell-Sakyi and Attoui, 2013 ; Shaw et al, 2018 ; O’Neal et al, 2020 ; Samaddar et al, 2020 ; Bonnet and Pollet, 2021 ; Narasimhan et al, 2021 ). To what extent these factors limit colonization and/or survival is not clear, but are undoubtedly pressures that must be coped with by the pathogen.…”

Section: Colonization: Overcoming Barriersmentioning

confidence: 99%