Microbiomes of Blood-Feeding Arthropods: Genes Coding for Essential Nutrients and Relation to Vector Fitness and Pathogenic Infections. A Review

Sonenshine, Daniel E.; Stewart, Philip E.

doi:10.3390/microorganisms9122433

Cited by 19 publications

(19 citation statements)

References 91 publications

(119 reference statements)

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“…Insect intestinal microbiota plays different roles such as gut cell proliferation, nutrient digestion and supplementation and toxin catabolism [38,[45][46][47][48]. Our results support the idea that this crosstalk between SLIMP and the commensal microbiota is capable to promote a very selective interference of the insect host in the microbial intestinal community, by the specific enrichment of the Bacteroidetes phylum (Fig.…”

Section: Discussionsupporting

confidence: 83%

An Aedes aegypti seryl-tRNA synthetase paralog controls bacteroidetes growth in the midgut

Silveira

Talyuli

Walter-Nuno

et al. 2022

Preprint

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Insect gut microbiota plays important roles in host physiology, such as nutrition, digestion, development, fertility, and immunity. We have found that in the intestine of Aedes aegypti, SLIMP (seryl-tRNA synthetase like insect mitochondrial protein) knockdown followed by a blood meal promotes dysbiosis, characterized by the overgrowth of a specific bacterial phylum, Bacteroidetes. In turn, the latter decreased both infection rates and Zika virus prevalence in the mosquitoes. Previous work in Drosophila melanogaster showed that SLIMP is involved in protein synthesis and mitochondrial respiration in a network directly coupled to mtDNA levels. There are no other reports on this enzyme and its function in other insect species. Our work expands the knowledge of the role of these SerRS paralogs. We show that A. aegypti SLIMP (AaeSLIMP) clusters with SLIMPs of the Nematocera sub-order, which have lost both the tRNA binding domain and active site residues, rendering them unable to activate amino acids and aminoacylate tRNAs. Knockdown of AaeSLIMP did not significantly influence the mosquitoes’ survival, oviposition, or eclosion. It also neither affected midgut cell respiration nor mitochondrial ROS production. However, it caused dysbiosis, which led to the activation of Dual oxidase and resulted in increased midgut ROS levels. Our data indicate that the intestinal microbiota can be controlled in a blood-feeding vector by a novel, unprecedent mechanism, impacting also mosquito vectorial competence towards zika virus and possibly other pathogens as well.

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Section: Discussionsupporting

confidence: 83%

An Aedes aegypti seryl-tRNA synthetase paralog controls bacteroidetes growth in the midgut

Silveira

Talyuli

Walter-Nuno

et al. 2022

Preprint

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“…An earlier study by Zhang et al (2016) demonstrated that B. burgdorferi does not require thiamine or Vitamin B1, a key cofactor for most living organisms, for its growth and replication and that it may have evolved to live in a Vitamin B-constrained environment of the tick. Sonenshine and Stewart (2021) also raise the possibility that environmental bacteria that form the bulk of the ectosymbionts found in the midgut milieu are also capable of providing essential aminoacids, metabolites and vitamins to the tick and hence influence tick fitness and in-turn the vectorial capacity of the tick. Narasimhan et al (2014) have shown that changes in the environmental microbiota composition influence larval engorgement and B. burgdorferi colonization of the tick.…”

Section: Tick-b Burgdorferi-commensal Microbiota Interactionsmentioning

confidence: 99%

The environment, the tick, and the pathogen – It is an ensemble

Couret

Schofield

Narasimhan

2022

Front. Cell. Infect. Microbiol.

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Ixodes scapularis is one of the predominant vectors of Borrelia burgdorferi, the agent of Lyme disease in the USA. The geographic distribution of I. scapularis, endemic to the northeastern and northcentral USA, is expanding as far south as Georgia and Texas, and northwards into Canada and poses an impending public health problem. The prevalence and spread of tick-borne diseases are influenced by the interplay of multiple factors including microbiological, ecological, and environmental. Molecular studies have focused on interactions between the tick-host and pathogen/s that determine the success of pathogen acquisition by the tick and transmission to the mammalian host. In this review we draw attention to additional critical environmental factors that impact tick biology and tick-pathogen interactions. With a focus on B. burgdorferi we highlight the interplay of abiotic factors such as temperature and humidity as well as biotic factors such as environmental microbiota that ticks are exposed to during their on- and off-host phases on tick, and infection prevalence. A molecular understanding of this ensemble of interactions will be essential to gain new insights into the biology of tick-pathogen interactions and to develop new approaches to control ticks and tick transmission of B. burgdorferi, the agent of Lyme disease.

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“…The at least 27 groups of peptide and protein salivary components of the Ixodidae comprise various members of the lipocalin, Kunitz domain, cystatin, basic tail, ixostatin, and metalloprotease families [42]. In addition, the composition can change significantly due to pathogen colonization [30,32,[43][44][45], and there even appears to be considerable interindividual variability among ticks of a single species, as demonstrated in Ixodes ricinus [46]. Ticks produce possibly the most complex saliva of all animals [47].…”

Section: Feeding and Salivary Secretionmentioning

confidence: 99%

The tick and I: Parasite‐host interactions between ticks and humans

Schön

2022

J Deutsche Derma Gesell

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Summary Ticks, particularly hard ticks (Ixodidae), which are among the most important vectors of dangerous infectious agents, feed on their hosts for extended periods of time. With this lifestyle, numerous adaptations have evolved in ticks and their hosts, the pharmacological importance of which is increasingly being recognized. Many bioactive substances in tick saliva are being considered as the basis of new drugs. For example, components of tick cement can be developed into tissue adhesives or wound closures. Analgesic and antipruritic salivary components inhibit histamine or bradykinin, while other tick‐derived molecules bind opioid or cannabinoid receptors. Tick saliva inhibits the extrinsic, intrinsic, or common pathway of blood coagulation with implications for the treatment of thromboembolic diseases. It contains vasodilating substances and affects wound healing. The broad spectrum of immunomodulatory and immunosuppressive effects of tick saliva, such as inhibition of chemokines or cellular immune responses, allows development of drugs against inflammation in autoimmune diseases and/or infections. Finally, modern vaccines against ticks can curb the spread of serious infections. The medical importance of the complex tick‐host interactions is increasingly being recognized and translated into first clinical applications. Using selected examples, an overview of the mutual adaptations of ticks and hosts is given here, focusing on their significance to medical advance.

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Microbiomes of Blood-Feeding Arthropods: Genes Coding for Essential Nutrients and Relation to Vector Fitness and Pathogenic Infections. A Review

Cited by 19 publications

References 91 publications

An Aedes aegypti seryl-tRNA synthetase paralog controls bacteroidetes growth in the midgut

An Aedes aegypti seryl-tRNA synthetase paralog controls bacteroidetes growth in the midgut

The environment, the tick, and the pathogen – It is an ensemble

The tick and I: Parasite‐host interactions between ticks and humans

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