Coculturing of Mosquito‐Microbiome Bacteria Promotes Heme Degradation in <i>Elizabethkingia anophelis</i>

Ganley, Jack G.; D’Ambrosio, Hannah K.; Shieh, Meg; Derbyshire, Emily R.

doi:10.1002/cbic.201900675

Cited by 15 publications

(20 citation statements)

References 62 publications

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“…A notable 112 predicted proteins identified in the genome of mosquito-associated strains of E. anophelis were annotated to features involved in resistance to antibiotics or other toxic compounds ( Kukutla et al, 2013 ). Indeed, in recent surveys of antibiotic-resistant bacteria in the mosquito microbiome, isolates of Elizabethkingia were identified to possess multi-drug resistance against ampicillin, carbenicillin, gentamycin, tetracycline, and kanamycin ( Hyde et al, 2019b ; Ganley, 2020 ). It is not clear what, if any, role this multi-drug resistance may play in colonizing the mosquito host, other than a potential fitness advantage against other bacteria making up the mosquito microbiome.…”

Section: A Path Forward: a Most Wanted List For Microbes In Gnotobiotic Studiesmentioning

confidence: 99%

“…This activity presumably facilitates blood digestion in the mosquito but also produced a metabolite of the class biliverdin, which may inhibit Pseudomonas growth. In this manner, E. anophelis gains a competitive advantage and may indirectly benefit the mosquito host ( Ganley, 2020 ). These observations all point to the importance of viewing the mosquito microbiome as a community and taking a population ecology viewpoint when linking the status of the mosquito microbiome to host phenotypes.…”

Section: Community Ecology and Microbiome Interactionsmentioning

confidence: 99%

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The Axenic and Gnotobiotic Mosquito: Emerging Models for Microbiome Host Interactions

et al. 2021

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The increasing availability of modern research tools has enabled a revolution in studies of non-model organisms. Yet, one aspect that remains difficult or impossible to control in many model and most non-model organisms is the presence and composition of the host-associated microbiota or the microbiome. In this review, we explore the development of axenic (microbe-free) mosquito models and what these systems reveal about the role of the microbiome in mosquito biology. Additionally, the axenic host is a blank template on which a microbiome of known composition can be introduced, also known as a gnotobiotic organism. Finally, we identify a “most wanted” list of common mosquito microbiome members that show the greatest potential to influence host phenotypes. We propose that these are high-value targets to be employed in future gnotobiotic studies. The use of axenic and gnotobiotic organisms will transition the microbiome into another experimental variable that can be manipulated and controlled. Through these efforts, the mosquito will be a true model for examining host microbiome interactions.

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Section: A Path Forward: a Most Wanted List For Microbes In Gnotobiotic Studiesmentioning

confidence: 99%

Section: Community Ecology and Microbiome Interactionsmentioning

confidence: 99%

The Axenic and Gnotobiotic Mosquito: Emerging Models for Microbiome Host Interactions

et al. 2021

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“…Serratia marcescens contributes to erythrocytes lysis by producing hemolysins in Anopheles mosquito 6 . Elizabethkingia anopheles possesses the heme-binding protein, HemS, that oxidatively cleaves heme to biliverdin 7 . Acinetobacter isolates in Aedes albopictus are able to metabolize blood component, α-keto-valeric acid and glycine, and improve blood digestion 8 .…”

Section: Introductionmentioning

confidence: 99%

Microbial tryptophan catabolism affects the vector competence ofAnopheles

Feng

Peng

Wen

et al. 2021

Preprint

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The influence of microbiota on mosquito physiology and vector competence is becoming increasingly clear but our understanding of interactions between microbiota and mosquitoes still remains incomplete. Here we show that gut microbiota of Anopheles stephensi, a competent malaria vector, participates mosquito tryptophan metabolism. Elimination of microbiota by antibiotics treatment leads to the accumulation of tryptophan (Trp) and its metabolites, kynurenine (Kyn), 3-hydroxykynurenine (3-HK) and xanthurenic acid (XA). Of these, 3-HK impairs the structure of peritrophic matrix (PM), thereby promoting Plasmodium berghei infection. Among the major gut microbiota in An. stephensi, Pseudomonas alcaligenes plays a role in catabolizing 3-HK as revealed by whole genome sequencing and LC-MS metabolic analysis. The genome of P. alcaligenes encodes kynureninase (KynU) that is responsible for the conversion of 3-HK to 3-Hydroxyanthranilic acid (3-HAA). Mutation of this gene abrogates the ability of P. alcaligenes to metabolize 3-HK, which in turn abolishes its role on PM protection. Colonization of An. stephensi with KynU mutated P. alcaligenes fails to protect mosquitoes against parasite infection as effectively as those with wild type bacterium. In summary, we identify an unexpected function of gut microbiota in controlling mosquito tryptophan metabolism with the major consequences on vector competence.

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“…Elizabethkingia was shown to be capable of inhibiting Pseudomonas , another mosquito-associated bacterium, via an antimicrobial independent mechanism (Ganley et al, 2020). Indeed, Elizabethkingia has broad antibiotic resistance because of a large number of genes encoding efflux pumps and β-lactamases present in its genome (Kukutla et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites

Mosquera

Villegas

Fernandes

et al. 2022

Preprint

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Aedes aegypti, the main vector of multiple arboviruses, is highly associated with human dwellings. Females exhibit an opportunistic oviposition behavior, seldomly laying eggs on natural containers, but rather distributing them among human-generated breeding sites. Bacterial communities associated with such sites, as well as the compositional shifts they undergo through the development of larval stages, have been described. Some bacteria can play a direct role in supporting the success of mosquito development. Additionally, exposure to different bacteria during larval phases can have an impact on life-history traits. Whether the larvae acquire symbionts from aquatic niches, or just require bacteria as food, is still debated. Based on these facts, we hypothesized that female Ae. aegypti shape the bacterial communities of breeding sites during oviposition as a form of niche construction to favor offspring fitness. Our study presents a series of experiments to address whether gravid females modify bacterial consortia present in larval habitats. For this, we first verified if females can mechanically transfer bacteria into culture media. As evidence of mechanical transmission was obtained, we then elaborated an experimental scheme to dissect effects from factors related to the act of oviposition and mosquito-egg-water interactions. The DNA samples obtained from breeding site water aliquots pertaining to five treatments were subjected to amplicon-oriented sequencing to infer their bacterial community structure. Microbial ecology analyses revealed significant differences between treatments in terms of diversity. Particularly, between-treatment shifts in abundance profiles were detected (pairwise PERMANOVA), also showing that females induce a significant decrease in alpha diversity (1-Simpson s index) through oviposition. In addition, indicator species analysis pinpointed bacterial taxa with significant predicting values and fidelity coefficients for the samples in which single females laid eggs. Furthermore, we provide evidence regarding how one of these indicator taxa, Elizabethkingia, exerts a positive effect upon the development and fitness of mosquito larvae, thus suggesting that the developmental niche construction hypothesis may hold true in this model.

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Coculturing of Mosquito‐Microbiome Bacteria Promotes Heme Degradation in Elizabethkingia anophelis

Cited by 15 publications

References 62 publications

The Axenic and Gnotobiotic Mosquito: Emerging Models for Microbiome Host Interactions

The Axenic and Gnotobiotic Mosquito: Emerging Models for Microbiome Host Interactions

Microbial tryptophan catabolism affects the vector competence ofAnopheles

Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites

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