Transcriptomic analysis reveals pronounced changes in gene expression due to sub-lethal pyrethroid exposure and ageing in insecticide resistance Anopheles coluzzii

Abstract Background Malaria control is heavily reliant on the use of insecticides that target and kill the adult female Anopheline vector. The intensive use of insecticides of the pyrethroid class has led to widespread resistance in mosquito populations. The intensity of pyrethroid resistance in som...

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Main Authors: V. A. Ingham, F. Brown, H. Ranson
Format: Article
Language:English
Published: BMC 2021-05-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-021-07646-7
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spelling doaj-acacf084c90542bf983835741defb66c2021-05-11T14:53:15ZengBMCBMC Genomics1471-21642021-05-0122111310.1186/s12864-021-07646-7Transcriptomic analysis reveals pronounced changes in gene expression due to sub-lethal pyrethroid exposure and ageing in insecticide resistance Anopheles coluzziiV. A. Ingham0F. Brown1H. Ranson2Department of Vector Biology, Liverpool School of Tropical MedicineDepartment of Vector Biology, Liverpool School of Tropical MedicineDepartment of Vector Biology, Liverpool School of Tropical MedicineAbstract Background Malaria control is heavily reliant on the use of insecticides that target and kill the adult female Anopheline vector. The intensive use of insecticides of the pyrethroid class has led to widespread resistance in mosquito populations. The intensity of pyrethroid resistance in some settings in Africa means mosquitoes can contact bednets treated with this insecticide class multiple times with minimal mortality effects. Furthermore, both ageing and diel cycle have been shown to have large impacts on the resistance phenotype. Together, these traits may affect other aspects of vector biology controlling the vectorial capacity or fitness of the mosquito. Results Here we show that sublethal exposure of a highly resistant Anopheles coluzzii population originally from Burkina Faso to the pyrethroid deltamethrin results in large and sustained changes to transcript expression. We identify five clear patterns in the data showing changes to transcripts relating to: DNA repair, respiration, translation, behaviour and oxioreductase processes. Further, we highlight differential regulation of transcripts from detoxification families previously linked with insecticide resistance, in addition to clear down-regulation of the oxidative phosphorylation pathway both indicative of changes in metabolism post-exposure. Finally, we show that both ageing and diel cycle have major effects on known insecticide resistance related transcripts. Conclusion Sub-lethal pyrethroid exposure, ageing and the diel cycle results in large-scale changes in the transcriptome of the major malaria vector Anopheles coluzzii. Our data strongly supports further phenotypic studies on how transcriptional changes such as reduced expression of the oxidative phosphorylation pathway or pyrethroid induced changes to redox state might impact key mosquito traits, such as vectorial capacity and life history traits.https://doi.org/10.1186/s12864-021-07646-7Insecticide resistanceAnopheles coluzziiPyrethroidsTranscriptomeSub-lethal exposure
collection DOAJ
language English
format Article
sources DOAJ
author V. A. Ingham
F. Brown
H. Ranson
spellingShingle V. A. Ingham
F. Brown
H. Ranson
Transcriptomic analysis reveals pronounced changes in gene expression due to sub-lethal pyrethroid exposure and ageing in insecticide resistance Anopheles coluzzii
BMC Genomics
Insecticide resistance
Anopheles coluzzii
Pyrethroids
Transcriptome
Sub-lethal exposure
author_facet V. A. Ingham
F. Brown
H. Ranson
author_sort V. A. Ingham
title Transcriptomic analysis reveals pronounced changes in gene expression due to sub-lethal pyrethroid exposure and ageing in insecticide resistance Anopheles coluzzii
title_short Transcriptomic analysis reveals pronounced changes in gene expression due to sub-lethal pyrethroid exposure and ageing in insecticide resistance Anopheles coluzzii
title_full Transcriptomic analysis reveals pronounced changes in gene expression due to sub-lethal pyrethroid exposure and ageing in insecticide resistance Anopheles coluzzii
title_fullStr Transcriptomic analysis reveals pronounced changes in gene expression due to sub-lethal pyrethroid exposure and ageing in insecticide resistance Anopheles coluzzii
title_full_unstemmed Transcriptomic analysis reveals pronounced changes in gene expression due to sub-lethal pyrethroid exposure and ageing in insecticide resistance Anopheles coluzzii
title_sort transcriptomic analysis reveals pronounced changes in gene expression due to sub-lethal pyrethroid exposure and ageing in insecticide resistance anopheles coluzzii
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2021-05-01
description Abstract Background Malaria control is heavily reliant on the use of insecticides that target and kill the adult female Anopheline vector. The intensive use of insecticides of the pyrethroid class has led to widespread resistance in mosquito populations. The intensity of pyrethroid resistance in some settings in Africa means mosquitoes can contact bednets treated with this insecticide class multiple times with minimal mortality effects. Furthermore, both ageing and diel cycle have been shown to have large impacts on the resistance phenotype. Together, these traits may affect other aspects of vector biology controlling the vectorial capacity or fitness of the mosquito. Results Here we show that sublethal exposure of a highly resistant Anopheles coluzzii population originally from Burkina Faso to the pyrethroid deltamethrin results in large and sustained changes to transcript expression. We identify five clear patterns in the data showing changes to transcripts relating to: DNA repair, respiration, translation, behaviour and oxioreductase processes. Further, we highlight differential regulation of transcripts from detoxification families previously linked with insecticide resistance, in addition to clear down-regulation of the oxidative phosphorylation pathway both indicative of changes in metabolism post-exposure. Finally, we show that both ageing and diel cycle have major effects on known insecticide resistance related transcripts. Conclusion Sub-lethal pyrethroid exposure, ageing and the diel cycle results in large-scale changes in the transcriptome of the major malaria vector Anopheles coluzzii. Our data strongly supports further phenotypic studies on how transcriptional changes such as reduced expression of the oxidative phosphorylation pathway or pyrethroid induced changes to redox state might impact key mosquito traits, such as vectorial capacity and life history traits.
topic Insecticide resistance
Anopheles coluzzii
Pyrethroids
Transcriptome
Sub-lethal exposure
url https://doi.org/10.1186/s12864-021-07646-7
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