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A symbiotic gut bacterium enhances Aedes albopictus resistance to insecticide

BACKGROUND: The increasing insecticide resistance of Aedes albopictus puts many countries in Asia and Africa, including China, at great risk of a mosquito-borne virus epidemic. To date, a growing number of researches have focused on the relationship between intestinal symbiotic bacteria and their ho...

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Autores principales: Wang, Haiyang, Liu, Hongmei, Peng, Hui, Wang, Yang, Zhang, Chongxing, Guo, Xiuxia, Wang, Haifang, Liu, Lijuan, Lv, Wenxiang, Cheng, Peng, Gong, Maoqing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8896681/
https://www.ncbi.nlm.nih.gov/pubmed/35245311
http://dx.doi.org/10.1371/journal.pntd.0010208
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author Wang, Haiyang
Liu, Hongmei
Peng, Hui
Wang, Yang
Zhang, Chongxing
Guo, Xiuxia
Wang, Haifang
Liu, Lijuan
Lv, Wenxiang
Cheng, Peng
Gong, Maoqing
author_facet Wang, Haiyang
Liu, Hongmei
Peng, Hui
Wang, Yang
Zhang, Chongxing
Guo, Xiuxia
Wang, Haifang
Liu, Lijuan
Lv, Wenxiang
Cheng, Peng
Gong, Maoqing
author_sort Wang, Haiyang
collection PubMed
description BACKGROUND: The increasing insecticide resistance of Aedes albopictus puts many countries in Asia and Africa, including China, at great risk of a mosquito-borne virus epidemic. To date, a growing number of researches have focused on the relationship between intestinal symbiotic bacteria and their hosts’ resistance to insecticides. This provides a novel aspect to the study of resistant mechanisms. METHODS/FINDINGS: This study reveals significant composition and dynamic changes in the intestinal symbiotic bacteria of Ae. albopictus between the resistant and susceptible strains based on full-length sequencing technology. The relative abundance of Serratia oryzae was significantly higher in the resistance strain than in the susceptible strains; also, the relative abundance of S. oryzae was significantly higher in deltamethrin-induced Ae. albopictus than in their counterpart. These suggested that S. oryzae may be involved in the development of insecticide resistance in Ae. albopictus. To explore the insecticide resistance mechanism, adult mosquitoes were fed with GFP-tagged S. oryzae, which resulted in stable bacterial enrichment in the mosquito gut without affecting the normal physiology, longevity, oviposition, and hatching rates of the host. The resistance measurements were made based on bioassays as per the WHO guidelines. The results showed that the survival rate of S. oryzae-enriched Ae. albopictus was significantly higher than the untreated mosquitoes, indicating the enhanced resistance of S. oryzae-enriched Ae. albopictus. Also, the activities of three metabolic detoxification enzymes in S. oryzae-enriched mosquitoes were increased to varying degrees. Meanwhile, the activity of extracellular enzymes released by S. oryzae was measured, but only carboxylesterase activity was detected. HPLC and UHPLC were respectively used to measure deltamethrin residue concentration and metabolite qualitative analysis, showing that the deltamethrin degradation efficiency of S. oryzae was positively correlated with time and bacterial amount. Deltamethrin was broken down into 1-Oleoyl-2-hydroxy-sn-glycero-3-PE and 2’,2’-Dibromo-2’-deoxyguanosine. Transcriptome analysis revealed that 9 cytochrome P450s, 8 GSTs and 7 CarEs genes were significantly upregulated. CONCLUSIONS: S. oryzae can be accumulated into adult Ae. albopictus by artificial feeding, which enhances deltamethrin resistance by inducing the metabolic detoxification genes and autocrine metabolic enzymes. S. oryzae is vertically transmitted in Ae. albopictus population. Importantly, S. oryzae can degrade deltamethrin in vitro, and use deltamethrin as the sole carbon source for their growths. Therefore, in the future, S. oryzae may also be commercially used to break down the residual insecticides in the farmland and lakes to protect the environment.
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spelling pubmed-88966812022-03-05 A symbiotic gut bacterium enhances Aedes albopictus resistance to insecticide Wang, Haiyang Liu, Hongmei Peng, Hui Wang, Yang Zhang, Chongxing Guo, Xiuxia Wang, Haifang Liu, Lijuan Lv, Wenxiang Cheng, Peng Gong, Maoqing PLoS Negl Trop Dis Research Article BACKGROUND: The increasing insecticide resistance of Aedes albopictus puts many countries in Asia and Africa, including China, at great risk of a mosquito-borne virus epidemic. To date, a growing number of researches have focused on the relationship between intestinal symbiotic bacteria and their hosts’ resistance to insecticides. This provides a novel aspect to the study of resistant mechanisms. METHODS/FINDINGS: This study reveals significant composition and dynamic changes in the intestinal symbiotic bacteria of Ae. albopictus between the resistant and susceptible strains based on full-length sequencing technology. The relative abundance of Serratia oryzae was significantly higher in the resistance strain than in the susceptible strains; also, the relative abundance of S. oryzae was significantly higher in deltamethrin-induced Ae. albopictus than in their counterpart. These suggested that S. oryzae may be involved in the development of insecticide resistance in Ae. albopictus. To explore the insecticide resistance mechanism, adult mosquitoes were fed with GFP-tagged S. oryzae, which resulted in stable bacterial enrichment in the mosquito gut without affecting the normal physiology, longevity, oviposition, and hatching rates of the host. The resistance measurements were made based on bioassays as per the WHO guidelines. The results showed that the survival rate of S. oryzae-enriched Ae. albopictus was significantly higher than the untreated mosquitoes, indicating the enhanced resistance of S. oryzae-enriched Ae. albopictus. Also, the activities of three metabolic detoxification enzymes in S. oryzae-enriched mosquitoes were increased to varying degrees. Meanwhile, the activity of extracellular enzymes released by S. oryzae was measured, but only carboxylesterase activity was detected. HPLC and UHPLC were respectively used to measure deltamethrin residue concentration and metabolite qualitative analysis, showing that the deltamethrin degradation efficiency of S. oryzae was positively correlated with time and bacterial amount. Deltamethrin was broken down into 1-Oleoyl-2-hydroxy-sn-glycero-3-PE and 2’,2’-Dibromo-2’-deoxyguanosine. Transcriptome analysis revealed that 9 cytochrome P450s, 8 GSTs and 7 CarEs genes were significantly upregulated. CONCLUSIONS: S. oryzae can be accumulated into adult Ae. albopictus by artificial feeding, which enhances deltamethrin resistance by inducing the metabolic detoxification genes and autocrine metabolic enzymes. S. oryzae is vertically transmitted in Ae. albopictus population. Importantly, S. oryzae can degrade deltamethrin in vitro, and use deltamethrin as the sole carbon source for their growths. Therefore, in the future, S. oryzae may also be commercially used to break down the residual insecticides in the farmland and lakes to protect the environment. Public Library of Science 2022-03-04 /pmc/articles/PMC8896681/ /pubmed/35245311 http://dx.doi.org/10.1371/journal.pntd.0010208 Text en © 2022 Wang et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Wang, Haiyang
Liu, Hongmei
Peng, Hui
Wang, Yang
Zhang, Chongxing
Guo, Xiuxia
Wang, Haifang
Liu, Lijuan
Lv, Wenxiang
Cheng, Peng
Gong, Maoqing
A symbiotic gut bacterium enhances Aedes albopictus resistance to insecticide
title A symbiotic gut bacterium enhances Aedes albopictus resistance to insecticide
title_full A symbiotic gut bacterium enhances Aedes albopictus resistance to insecticide
title_fullStr A symbiotic gut bacterium enhances Aedes albopictus resistance to insecticide
title_full_unstemmed A symbiotic gut bacterium enhances Aedes albopictus resistance to insecticide
title_short A symbiotic gut bacterium enhances Aedes albopictus resistance to insecticide
title_sort symbiotic gut bacterium enhances aedes albopictus resistance to insecticide
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8896681/
https://www.ncbi.nlm.nih.gov/pubmed/35245311
http://dx.doi.org/10.1371/journal.pntd.0010208
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