A symbiotic gut bacterium enhances Aedes albopictus resistance to insecticide

Abstract

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.

Isolation, characterization and functional analysis of a bacteriophage targeting Culex pipiens pallens resistance-associated Aeromonas hydrophila

“…pipiens in mosquito control operation areas [ 48 , 49 ]. Recent studies have indicated that symbiotic bacteria enhance mosquito resistance by directly breaking down the insecticide and increasing their metabolic enzyme activity [ 6 , 9 ]. Nonetheless, the impact of symbiotic bacteria on target site susceptibility has not been investigated.…”

“…There are notable disparities in the composition of intestinal microbial communities between insecticide-sensitive and -resistant mosquitoes. Asiaia and Serratia bacteria have been observed to contribute to the development of mosquito sensitivity to deltamethrin; for example, Serratia oryzae can significantly enhance the resistance of Aedes albopictus to deltamethrin by upregulating the expression of metabolic detoxification genes [ 6 , 7 ]. Our previous study identified Aeromonas hydrophila as the predominant bacterial species in the intestinal tract of a deltamethrin-resistant strain of Cx.…”

Pesticide resistance in arthropods: Ecology matters too

“…Differences between generalists and specialists are also observed at the molecular level. For example neofunctionalisation of gene copies and horizontal gene transfer often enhances genomic flexibility in generalists to facilitate diverse host usages (Heidel-Fischer et al, 2019;Kirsch et al, 2014;Prasad et al, 2021;Wybouw et al, 2015). In addition, the genomes of polyphagous species often show dramatic expansion of chemosensory and detoxifying gene repertoire resulting in more remarkable plasticity during herbivory, which often accounts for the observed difference in the diet breadth between generalist and specialist insects (Grbić et al, 2011;Li et al, 2013;Xu et al, 2016).…”

“…Herbivorous arthropods harbour gut microbiota that has been suggested to aid in plant allelochemical detoxification (Ceja‐Navarro et al, 2015; Després et al, 2007; Francoeur et al, 2020) even if its importance may vary between insect orders (Hammer et al, 2017). Endosymbionts have recently been shown to aid their arthropod host in detoxifying pesticides, but this area is still largely unexplored (Almeida et al 2017; Itoh et al, 2018; Le Goff & Giraudo, 2019; Wang et al, 2022). Gut microbiota may thus provide a phenocopy of cross‐resistance and the possibility for both horizontal and lateral transfer of microbe‐mediated resistance between individual arthropods (Acuna et al, 2012; Cheng et al, 2018; Rassati et al, 2019; Taerum et al, 2013).…”

Cereal leaf beetle‐associated bacteria enhance the survival of their host upon insecticide treatments and respond differently to insecticides with different modes of action

“…Due to the indiscriminate use of insecticides over the years, herbivorous insects, including CLB, have developed insecticide resistance (Tanasković et al, 2012 ). Several beetles adaptations have been identified to explain the reduced efficiency of insecticides, including (a) mutation of insecticide action sites (Obrępalska‐Stęplowska et al, 2016 ; Wrzesińska et al, 2014 ), (b) thickening of insect epidermis reducing insecticide penetration (Hemingway & Karunaratne, 1998 ; Rocha et al, 2021 ; South & Hastings, 2018 ; Wang et al, 2022 ), (c) increase in insecticide metabolism through up‐regulation of genes encoding enzymes such as cytochrome P450, monooxygenase, glutathione S‐transferase, carboxylesterase, acetylcholinesterase, hydrolase and many more associated with insecticide degradation (Chang et al, 2017 ; Cisse et al, 2015 ; Jaffar et al, 2022 ; Vontas et al, 2020 ; Wang et al, 2022 ; Wieczorek et al, 2014 ). The implication of symbiotic microbes as potential contributors to insecticide resistance is of great interest.…”