Abstract
Iron and copper chelation restricts Plasmodium growth in vitro and in mammalian hosts. The parasite alters metal homeostasis in red blood cells to its favor, for example metabolizing hemoglobin to hemozoin. Metal interactions with the mosquito have not, however, been studied. Here, we describe the metallomes of Anopheles albimanus and Aedes aegypti throughout their life cycle and following a blood meal. Consistent with previous reports, we found evidence of maternal iron deposition in embryos of Ae. aegypti, but less so in An. albimanus. Sodium, potassium, iron, and copper are present at higher concentrations during larval developmental stages. Two An. albimanus phenotypes that differ in their susceptibility to Plasmodium berghei infection were studied. The susceptible white stripe (ws) phenotype was named after a dorsal white stripe apparent during larval stages 3, 4, and pupae. During larval stage 3, ws larvae accumulate more iron and copper than the resistant brown stripe (bs) phenotype counterparts. A similar increase in copper and iron accumulation was also observed in the susceptible ws, but not in the resistant bs phenotype following P. berghei infection. Feeding ws mosquitoes with extracellular iron and copper chelators before and after receiving Plasmodium-infected blood protected from infection and simultaneously affected follicular development in the case of iron chelation. Unexpectedly, the application of the iron chelator to the bs strain reverted resistance to infection. Besides a drop in iron, iron-chelated bs mosquitoes experienced a concomitant loss of copper. Thus, the effect of metal chelation on P. berghei infectivity was strain-specific.
Highlights
The role of mosquitoes as vectors of different diseases has long been recognized [1]
We asked whether susceptibility to Plasmodium infection correlated with a differential response in mosquito metal homeostasis
We tested the effects of iron and copper chelation treatment of adult mosquitoes concerning propensity of infection and mosquito reproduction
Summary
The role of mosquitoes as vectors of different diseases has long been recognized [1]. A thorough characterization of the physiological interactions between viruses or parasites and their insect hosts could further inform the design of interventions to interrupt infections in affected areas [7,8]. One such relatively unexplored area of insect physiology–with the possible exception of studies in the model organism Drosophila melanogaster [9,10,11,12,13]–is metal metabolism. Several studies exist for iron metabolism in mosquitoes (reviewed in [14]), including characterizations of the iron storage ferritin complex [15], the iron trafficking transferrin protein [16], and iron regulatory proteins [17] in Aedes aegypti. Heme oxygenase was described in Anopheles gambiae [22] and Ae. aegypti [23]
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