Deleterious Effects of Neonicotinoid Pesticides on <named-content content-type="genus-species">Drosophila melanogaster</named-content> Immune Pathways

ABSTRACT Neonicotinoid insecticides are common agrochemicals that are used to kill pest insects and improve crop yield. However, sublethal exposure can exert unintentional toxicity to honey bees and other beneficial pollinators by dysregulating innate immunity. Generation of hydrogen peroxide (H2O2)...

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Autores principales:	John A. Chmiel, Brendan A. Daisley, Jeremy P. Burton, Gregor Reid
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Drosophila Lactobacillus dual oxidase honey bee host-microbe interactions immune deficiency pathway Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5b1c8125ddc5463bb9b761a1836f8f1e
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spelling	oai:doaj.org-article:5b1c8125ddc5463bb9b761a1836f8f1e2021-11-15T15:59:40ZDeleterious Effects of Neonicotinoid Pesticides on <named-content content-type="genus-species">Drosophila melanogaster</named-content> Immune Pathways10.1128/mBio.01395-192150-7511https://doaj.org/article/5b1c8125ddc5463bb9b761a1836f8f1e2019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01395-19https://doaj.org/toc/2150-7511ABSTRACT Neonicotinoid insecticides are common agrochemicals that are used to kill pest insects and improve crop yield. However, sublethal exposure can exert unintentional toxicity to honey bees and other beneficial pollinators by dysregulating innate immunity. Generation of hydrogen peroxide (H2O2) by the dual oxidase (Duox) pathway is a critical component of the innate immune response, which functions to impede infection and maintain homeostatic regulation of the gut microbiota. Despite the importance of this pathway in gut immunity, the consequences of neonicotinoid exposure on Duox signaling have yet to be studied. Here, we use a Drosophila melanogaster model to investigate the hypothesis that imidacloprid (a common neonicotinoid) can affect the Duox pathway. The results demonstrated that exposure to sublethal imidacloprid reduced H2O2 production by inhibiting transcription of the Duox gene. Furthermore, the reduction in Duox expression was found to be a result of imidacloprid interacting with the midgut portion of the immune deficiency pathway. This impairment led to a loss of microbial regulation, as exemplified by a compositional shift and increased total abundance of Lactobacillus and Acetobacter spp. (dominant microbiota members) found in the gut. In addition, we demonstrated that certain probiotic lactobacilli could ameliorate Duox pathway impairment caused by imidacloprid, but this effect was not directly dependent on the Duox pathway itself. This study is the first to demonstrate the deleterious effects that neonicotinoids can have on Duox-mediated generation of H2O2 and highlights a novel coordination between two important innate immune pathways present in insects. IMPORTANCE Sublethal exposure to certain pesticides (e.g., neonicotinoid insecticides) is suspected to contribute to honey bee (Apis mellifera) population decline in North America. Neonicotinoids are known to interfere with immune pathways in the gut of insects, but the underlying mechanisms remain elusive. We used a Drosophila melanogaster model to understand how imidacloprid (a common neonicotinoid) interferes with two innate immune pathways—Duox and Imd. We found that imidacloprid dysregulates these pathways to reduce hydrogen peroxide production, ultimately leading to a dysbiotic shift in the gut microbiota. Intriguingly, we found that presupplementation with probiotic bacteria could mitigate the harmful effects of imidacloprid. Thus, these observations uncover a novel mechanism of pesticide-induced immunosuppression that exploits the interconnectedness of two important insect immune pathways.John A. ChmielBrendan A. DaisleyJeremy P. BurtonGregor ReidAmerican Society for MicrobiologyarticleDrosophilaLactobacillusdual oxidasehoney beehost-microbe interactionsimmune deficiency pathwayMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Drosophila Lactobacillus dual oxidase honey bee host-microbe interactions immune deficiency pathway Microbiology QR1-502
spellingShingle	Drosophila Lactobacillus dual oxidase honey bee host-microbe interactions immune deficiency pathway Microbiology QR1-502 John A. Chmiel Brendan A. Daisley Jeremy P. Burton Gregor Reid Deleterious Effects of Neonicotinoid Pesticides on <named-content content-type="genus-species">Drosophila melanogaster</named-content> Immune Pathways
description	ABSTRACT Neonicotinoid insecticides are common agrochemicals that are used to kill pest insects and improve crop yield. However, sublethal exposure can exert unintentional toxicity to honey bees and other beneficial pollinators by dysregulating innate immunity. Generation of hydrogen peroxide (H2O2) by the dual oxidase (Duox) pathway is a critical component of the innate immune response, which functions to impede infection and maintain homeostatic regulation of the gut microbiota. Despite the importance of this pathway in gut immunity, the consequences of neonicotinoid exposure on Duox signaling have yet to be studied. Here, we use a Drosophila melanogaster model to investigate the hypothesis that imidacloprid (a common neonicotinoid) can affect the Duox pathway. The results demonstrated that exposure to sublethal imidacloprid reduced H2O2 production by inhibiting transcription of the Duox gene. Furthermore, the reduction in Duox expression was found to be a result of imidacloprid interacting with the midgut portion of the immune deficiency pathway. This impairment led to a loss of microbial regulation, as exemplified by a compositional shift and increased total abundance of Lactobacillus and Acetobacter spp. (dominant microbiota members) found in the gut. In addition, we demonstrated that certain probiotic lactobacilli could ameliorate Duox pathway impairment caused by imidacloprid, but this effect was not directly dependent on the Duox pathway itself. This study is the first to demonstrate the deleterious effects that neonicotinoids can have on Duox-mediated generation of H2O2 and highlights a novel coordination between two important innate immune pathways present in insects. IMPORTANCE Sublethal exposure to certain pesticides (e.g., neonicotinoid insecticides) is suspected to contribute to honey bee (Apis mellifera) population decline in North America. Neonicotinoids are known to interfere with immune pathways in the gut of insects, but the underlying mechanisms remain elusive. We used a Drosophila melanogaster model to understand how imidacloprid (a common neonicotinoid) interferes with two innate immune pathways—Duox and Imd. We found that imidacloprid dysregulates these pathways to reduce hydrogen peroxide production, ultimately leading to a dysbiotic shift in the gut microbiota. Intriguingly, we found that presupplementation with probiotic bacteria could mitigate the harmful effects of imidacloprid. Thus, these observations uncover a novel mechanism of pesticide-induced immunosuppression that exploits the interconnectedness of two important insect immune pathways.
format	article
author	John A. Chmiel Brendan A. Daisley Jeremy P. Burton Gregor Reid
author_facet	John A. Chmiel Brendan A. Daisley Jeremy P. Burton Gregor Reid
author_sort	John A. Chmiel
title	Deleterious Effects of Neonicotinoid Pesticides on <named-content content-type="genus-species">Drosophila melanogaster</named-content> Immune Pathways
title_short	Deleterious Effects of Neonicotinoid Pesticides on <named-content content-type="genus-species">Drosophila melanogaster</named-content> Immune Pathways
title_full	Deleterious Effects of Neonicotinoid Pesticides on <named-content content-type="genus-species">Drosophila melanogaster</named-content> Immune Pathways
title_fullStr	Deleterious Effects of Neonicotinoid Pesticides on <named-content content-type="genus-species">Drosophila melanogaster</named-content> Immune Pathways
title_full_unstemmed	Deleterious Effects of Neonicotinoid Pesticides on <named-content content-type="genus-species">Drosophila melanogaster</named-content> Immune Pathways
title_sort	deleterious effects of neonicotinoid pesticides on <named-content content-type="genus-species">drosophila melanogaster</named-content> immune pathways
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/5b1c8125ddc5463bb9b761a1836f8f1e
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Deleterious Effects of Neonicotinoid Pesticides on <named-content content-type="genus-species">Drosophila melanogaster</named-content> Immune Pathways

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