The impact of metagenomic interplay on the mosquito redox homeostasis

Abstract

Mosquitoes are exposed to oxidative challenges throughout their life cycle. The primary challenge comes from a blood meal. The blood digestion turns the midgut into an oxidative environment, which imposes pressure not only on mosquito fecundity and other physiological traits but also on the microbiota in the midgut. During evolution, mosquitoes have developed numerous oxidative defense mechanisms to maintain redox homeostasis in the midgut. In addition to antioxidants, SOD, catalase, and glutathione system, sufficient supply of the reducing agent, NADPH, is vital for a successful defense against oxidative stress. Increasing evidence indicates that in response to oxidative stress, cells reconfigure metabolic pathways to increase the generation of NADPH through NADP-reducing networks including the pentose phosphate pathway and others. The microbial homeostasis is critical for the functional contributions to various host phenotypes. The symbiotic microbiota is regulated largely by the Duox-ROS pathway in Drosophila. In mosquitoes, Duox-ROS pathway, heme-mediated signaling, antimicrobial peptide production and C-type lectins work in concert to maintain the dynamic microbial community in the midgut. Microbial mechanisms against oxidative stress in this context are not well understood. Emerging evidence that microbial metabolites trigger host oxidative response warrants further study on the metagenomic interplay in an oxidative environment like mosquito gut ecosystem. Besides the classical Drosophila model, hematophagous insects like mosquitoes provide an alternative model system to study redox homeostasis in a symbiotic metagenomic context.

Proteomic Investigation on Anopheles gambiae in Burkina Faso Related to Insecticide Pressures from Different Climatic Regions

“…[ 45 ] Similarly, the redox homeostasis system (thioredoxin, GSH peroxidase…) plays a vital role in the dynamics of symbiotic microbiota, which impacts Plasmodium transmission. [ 46 ] This would result in important implications for the design of strategies aiming at interfering with the GSH redox‐system of the mosquito. [ 45 ]…”

Elizabethkingia anophelisresponse to iron stress: physiologic, genomic, and transcriptomic analyses

“…The female mosquito gut is characterized by slightly acidic pH with a tendency to alkalinity after blood meals, a small volume, and frequent nutritional fluctuations (41). Iron availability contributes importantly to the assemblage of microorganisms in the mosquito midgut (3, 19, 42). Bacterial inhabitants of the adult mosquito midgut experience extreme conditions with relationship to iron availability, either having insufficient supply prior to and between blood meals, or excessive free iron and associated free radicals during and after blood meals (42, 43).…”

“…Iron availability contributes importantly to the assemblage of microorganisms in the mosquito midgut (3, 19, 42). Bacterial inhabitants of the adult mosquito midgut experience extreme conditions with relationship to iron availability, either having insufficient supply prior to and between blood meals, or excessive free iron and associated free radicals during and after blood meals (42, 43). Our results showed that E. anophelis , a commensal organism of the mosquito midgut, responds to these extreme conditions and utilizes multiple iron uptake pathways, TBDTs, and iron chelating proteins in response to iron stress.…”

“…Hemoglobin remarkably attenuated the overproduction of ROS and NO, reverted mitochondrial membrane potential, and repressed caspase-3/7 (65). It is possible that the hemin/iron from degraded hemoglobin can immediately be transported into cells and incorporated to some of the heme-containing antioxidative enzymes (such as heme-containing catalases) when bacteria suffer the crisis of strong reactive oxygen radicals (42, 66). Similarly, some of the non-heme proteins (with iron as the cofactor) can remove the ROS (66).…”

Efflux pumps and antimicrobial resistance: Paradoxical components in systems genomics

“…Besides, their antimicrobial role, AMPs are also involved in chemotaxis and redox homeostasis with rapid radical scavenging ability (Cole et al, 2003;Com et al, 2003;Ganz, 2002;Liu et al, 2010;Zhao et al, 2011). Recently, the metagenomic approaches are extensively reviewed to explore the role of AMPs in redox homeostasis (Champion and Xu, 2017).…”