Reactive oxygen species detoxification by catalase is a major determinant of fecundity in the mosquito Anopheles gambiae

Abstract

The mosquito Anopheles gambiae is a primary vector of Plasmodium parasites in Africa. The effect of aging on reproductive output in A. gambiae females from three strains that differ in their ability to melanize Plasmodium and in their systemic levels of hydrogen peroxide (H2O2), a reactive oxygen species (ROS), was analyzed. The number of eggs oviposited after the first blood meal decreases with age in all strains; however, this decline was much more pronounced in the G3 (unselected) and R (refractory to Plasmodium infection) strains than in the S (highly susceptible to Plasmodium) strain. Reduction of ROS levels in G3 and R females by administration of antioxidants reversed this age-related decline in fecundity. The S and G3 strains were fixed for two functionally different catalase alleles that differ at the second amino acid position (Ser2Trp). Biochemical analysis of recombinant proteins revealed that the Trp isoform has lower specific activity and higher Km than the Ser isoform, indicating that the former is a less efficient enzyme. The Trp-for-Ser substitution appears to destabilize the functional tetrameric form of the enzyme. Both alleles are present in the R strain, and Ser/Ser females had significantly higher fecundity than Trp/Trp females. Finally, a systemic reduction in catalase activity by dsRNA-mediated knockdown significantly reduced the reproductive output of mosquito females, indicating that catalase plays a central role in protecting the oocyte and early embryo from ROS damage.insect ͉ malaria ͉ Plasmodium ͉ reproduction ͉ single-nucleotide polymorphism

Reactive Oxygen Species Modulate Anopheles gambiae Immunity against Bacteria and Plasmodium

“…of the ingested blood meal in mosquitoes in which catalase has been silenced is similar to that of the controls injected with dsRNA LacZ (28), indicating that the observed differences in infectivity cannot be explained by differences in blood-meal size. The reduction in infectivity after catalase silencing can already be observed 24 h PI and appears to be due to increased ookinete lysis (Fig.…”

“…It is interesting to note that, in contrast to their deleterious effect on immunity, the same antioxidants also have beneficial effects, as they significantly reduce age-related loss of fecundity in mosquitoes (28). These observations illustrate the importance of ROS in maintaining the balance between immunity and fecundity.…”

Molecular cloning and characterization of a catalase gene from Zhikong scallop Chlamys farreri

“…However, these advantages came at a cost: toxic by-products known as reactive oxygen species (ROS) were produced. The production of ROS was also one of the earliest cellular responses in aerobic organisms following successful pathogen recognition [1] or exposure to radiation, ultraviolet radiation, and some chemicals [2,3]. ROS can stimulate signal transduction pathways like NF-kB or MAPK [4e6], and mediate various responses such as cell growth and apoptosis [7,8], or be responsible for killing invading microorganisms [9].…”

The oxidative environment: a mediator of interspecies communication that drives symbiosis evolution

“…In the Anopheles-Plasmodium interaction, a state of chronic oxidative stress in the mosquito is indeed associated with both an increase in immune competence and a decrease in fecundity [48,49]. Hence, different strategies will be under selection to limit potential deleterious effects associated with symbiosis, depending on the initial cost for the host and the prevalence of the symbiont in the host population.…”