Abstract
Aedes aegypti mosquitoes transmit arboviruses of important global health impact, and their intestinal microbiota can influence vector competence by stimulating the innate immune system. Midgut epithelial cells also produce toxic reactive oxygen species (ROS) by dual oxidases (DUOXs) that are essential players in insect immunity. Strigomonas culicis is a monoxenous trypanosomatid that naturally inhabits mosquitoes; it hosts an endosymbiotic bacterium that completes essential biosynthetic pathways of the parasite and influences its oxidative metabolism. Our group previously showed that S. culicis hydrogen peroxide (H2O2)-resistant (WTR) strain is more infectious to A. aegypti mosquitoes than the wild-type (WT) strain. Here, we investigated the influence of both strains on the midgut oxidative environment and the effect of infection on mosquito fitness and immunity. WT stimulated the production of superoxide by mitochondrial metabolism of midgut epithelial cells after 4 days post-infection, while WTR exacerbated H2O2 production mediated by increased DUOX activity and impairment of antioxidant system. The infection with both strains also disrupted the fecundity and fertility of the females, with a greater impact on reproductive fitness of WTR-infected mosquitoes. The presence of these parasites induced specific transcriptional modulation of immune-related genes, such as attacin and defensin A during WTR infection (11.8- and 6.4-fold, respectively) and defensin C in WT infection (7.1-fold). Thus, we propose that A. aegypti oxidative response starts in early infection time and does not affect the survival of the H2O2-resistant strain, which has a more efficient antioxidant system. Our data provide new biological aspects of A. aegypti–S. culicis relationship that can be used later in alternative vector control strategies.
Highlights
Aedes aegypti is the primary vector of arboviruses, such as dengue, Zika, chikungunya, and urban yellow fever, which cause a heavy health burden and global economic losses (Lwande et al, 2020)
As DHE oxidation is known to yield two distinct products according to oxidative species available, the concentration of EOH and E (Zhao et al, 2003) in tissues 4 dpi was differentially assessed through High-Performance Liquid Chromatography (HPLC)
Our data pointed out that H2O2 was produced during S. culicis infection, increasing detection 1.8- and 7.0-fold after WT and wild-type H2O2-resistant (WTR) infections, respectively
Summary
Aedes aegypti is the primary vector of arboviruses, such as dengue, Zika, chikungunya, and urban yellow fever, which cause a heavy health burden and global economic losses (Lwande et al, 2020). The distribution of this vector and consequent transmission of these pathogens were for a long time restricted to particular regions. NADPH oxidases are important ROS producers in midgut epithelial cells of insects, dual oxidase (DUOX) This enzyme is responsible for generating hydrogen peroxide (H2O2) in response to a wide range of stimuli, being involved in diverse aspects of insects’ gut–microbe interactions (Kim and Lee, 2014). The activation of both regulatory pathways is necessary for the robust pro-oxidative response (Bai et al, 2021)
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