Gut microbiota in Drosophila melanogaster interacts with Wolbachia but does not contribute to Wolbachia -mediated antiviral protection

Ye, Yixin H.; Seleznev, Andrei; Flores, Heather A.; Woolfit, Megan; McGraw, Elizabeth A.

doi:10.1016/j.jip.2016.11.011

Cited by 52 publications

(48 citation statements)

References 65 publications

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“…Nevertheless, with the exception of Chryseobacterium , we were able to alter the nature and/or extent of these interactions by antibiotic treatment, without observing any effects on DENV susceptibility. Similar results were recently observed in Drosophila , where Wolbachia had significant interactions with the microbiome, but altering the microbiome composition by antibiotic treatment did not change susceptibility to Drosophila C virus [43]. These results suggest that Wolbachia’s interactions with the taxa identified in our study are unlikely to contribute to the anti-DENV phenotype in Ae .…”

Section: Discussionsupporting

confidence: 90%

The microbiome composition of Aedes aegypti is not critical for Wolbachia-mediated inhibition of dengue virus

Audsley

McGraw

2017

PLoS Negl Trop Dis

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BackgroundDengue virus (DENV) is primarily vectored by the mosquito Aedes aegypti, and is estimated to cause 390 million human infections annually. A novel method for DENV control involves stable transinfection of Ae. aegypti with the common insect endosymbiont Wolbachia, which mediates an antiviral effect. However, the mechanism by which Wolbachia reduces the susceptibility of Ae. aegypti to DENV is not fully understood. In this study we assessed the potential of resident microbiota, which can play important roles in insect physiology and immune responses, to affect Wolbachia-mediated DENV blocking.Methodology/FindingsThe microbiome of Ae. aegypti stably infected with Wolbachia strain wMel was compared to that of Ae. aegypti without Wolbachia, using 16s rDNA profiling. Our results indicate that although Wolbachia affected the relative abundance of several genera, the microbiome of both the Wolbachia-infected and uninfected mosquitoes was dominated by Elizabethkingia and unclassified Enterobacteriaceae. To assess the potential of the resident microbiota to affect the Wolbachia-mediated antiviral effect, we used antibiotic treatment before infection with DENV by blood-meal. In spite of a significant shift in the microbiome composition in response to the antibiotics, we detected no effect of antibiotic treatment on DENV infection rates, or on the DENV load of infected mosquitoes.Conclusions/SignificanceOur findings indicate that stable infection with Wolbachia strain wMel produces few effects on the microbiome of laboratory-reared Ae. aegypti. Moreover, our findings suggest that the microbiome can be significantly altered without affecting the fundamental DENV blocking phenotype in these mosquitoes. Since Ae. aegypti are likely to encounter diverse microbiota in the field, this is a particularly important result in the context of using Wolbachia as a method for DENV control.

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Section: Discussionsupporting

confidence: 90%

The microbiome composition of Aedes aegypti is not critical for Wolbachia-mediated inhibition of dengue virus

Audsley

McGraw

2017

PLoS Negl Trop Dis

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“…Wolbachia as intracellular and all others as gut residents in order to evaluate the effect of the transplantation, as described elsewhere. 64…”

Section: Statistical Analysesmentioning

confidence: 99%

Strong responses of Drosophila melanogaster microbiota to developmental temperature

Moghadam

Thorshauge

Kristensen

et al. 2017

Fly

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Physiological responses to changes in environmental conditions such as temperature may partly arise from the resident microbial community that integrates a wide range of bio-physiological aspects of the host. In the present study, we assessed the effect of developmental temperature on the thermal tolerance and microbial community of Drosophila melanogaster. We also developed a bacterial transplantation protocol in order to examine the possibility of reshaping the host bacterial composition and assessed its influence on the thermotolerance phenotype. We found that the temperature during development affected thermal tolerance and the microbial composition of male D. melanogaster. Flies that developed at low temperature (13°C) were the most cold resistant and showed the highest abundance of Wolbachia, while flies that developed at high temperature (31°C) were the most heat tolerant and had the highest abundance of Acetobacter. In addition, feeding newly eclosed flies with bacterial suspensions from intestines of flies developed at low temperatures changed the heat tolerance of recipient flies. However, we were not able to link this directly to a change in the host bacterial composition.

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“…A collective limitation of these studies is that the distinction between vitamin contributions by endosymbionts and gut microbiota have not been systematically confirmed as separate. Recent work indicates that antibiotic treatments restructure the gut microbiome in insects (Gendrin et al 2015; Ye et al 2016; Raymann et al 2017), as has also been seen in mammals (Antonopoulos et al 2009; Jernberg et al 2010; Buffie et al 2012). The implications of these treatments are unclear, as the gut microbiome is implicated in vitamin provisioning (Tatum 1939; Friend 1958; Blatch et al 2010; Piper et al 2014; Wong et al 2014; Nation 2015).…”

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confidence: 90%

Predictive Genomic Analyses Inform the Basis for Vitamin Metabolism and Provisioning in Bacteria-Arthropod Endosymbioses

Serbus

Rodriguez

Sharmin

et al. 2017

G3 Genes|Genomes|Genetics

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The requirement of vitamins for core metabolic processes creates a unique set of pressures for arthropods subsisting on nutrient-limited diets. While endosymbiotic bacteria carried by arthropods have been widely implicated in vitamin provisioning, the underlying molecular mechanisms are not well understood. To address this issue, standardized predictive assessment of vitamin metabolism was performed in 50 endosymbionts of insects and arachnids. The results predicted that arthropod endosymbionts overall have little capacity for complete de novo biosynthesis of conventional or active vitamin forms. Partial biosynthesis pathways were commonly predicted, suggesting a substantial role in vitamin provisioning. Neither taxonomic relationships between host and symbiont, nor the mode of host-symbiont interaction were clear predictors of endosymbiont vitamin pathway capacity. Endosymbiont genome size and the synthetic capacity of nonsymbiont taxonomic relatives were more reliable predictors. We developed a new software application that also predicted that last-step conversion of intermediates into active vitamin forms may contribute further to vitamin biosynthesis by endosymbionts. Most instances of predicted vitamin conversion were paralleled by predictions of vitamin use. This is consistent with achievement of provisioning in some cases through upregulation of pathways that were retained for endosymbiont benefit. The predicted absence of other enzyme classes further suggests a baseline of vitamin requirement by the majority of endosymbionts, as well as some instances of putative mutualism. Adaptation of this workflow to analysis of other organisms and metabolic pathways will provide new routes for considering the molecular basis for symbiosis on a comprehensive scale.

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Gut microbiota in Drosophila melanogaster interacts with Wolbachia but does not contribute to Wolbachia -mediated antiviral protection

Cited by 52 publications

References 65 publications

The microbiome composition of Aedes aegypti is not critical for Wolbachia-mediated inhibition of dengue virus

The microbiome composition of Aedes aegypti is not critical for Wolbachia-mediated inhibition of dengue virus

Strong responses of Drosophila melanogaster microbiota to developmental temperature

Predictive Genomic Analyses Inform the Basis for Vitamin Metabolism and Provisioning in Bacteria-Arthropod Endosymbioses

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