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Ambient temperature and dietary supplementation interact to shape mosquito vector competence for malaria.

ABSTRACT: The extent to which environmental factors influence the ability of Anopheles mosquitoes to transmit malaria parasites remains poorly explored. Environmental variation, such as change in ambient temperature, will not necessarily influence the rates of host and parasite processes equivalently, potentially resulting in complex effects on infection outcomes. As proof of principle, we used Anopheles stephensi and the rodent malaria parasite, Plasmodium yoelii, to examine the effects of a range of constant temperatures on one aspect of host defense (detected as alterations in expression of nitric oxide synthase gene - NOS) to parasite infection. We experimentally boosted mosquito midgut immunity to infection through dietary supplementation with the essential amino acid l-Arginine (l-Arg), which increases midgut nitric oxide (NO) levels by infection-induced NOS catalysis in A. stephensi. At intermediate temperatures, supplementation reduced oocyst prevalence, oocyst intensity, and sporozoite prevalence suggesting that the outcome of parasite infection was potentially dependent upon the rate of NOS-mediated midgut immunity. At low and high temperature extremes, however, infection was severely constrained irrespective of supplementation. The effects of l-Arg appeared to be mediated by NO-dependent negative feedback on NOS expression, as evidenced by depressed NOS expression in l-Arg treated groups at temperatures where supplementation decreased parasite infection. These results suggest the need to consider the direct (e.g. effects of mosquito body temperature on parasite physiology) and indirect effects (e.g. mediated through changes in mosquito physiology/immunity) of environmental factors on mosquito-malaria interactions in order to understand natural variation in vector competence.

SUBMITTER: Murdock CC

PROVIDER: S-EPMC4107084 | biostudies-literature | 2014 Aug

REPOSITORIES: biostudies-literature

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Ambient temperature and dietary supplementation interact to shape mosquito vector competence for malaria.

Murdock Courtney C CC Blanford Simon S Luckhart Shirley S Thomas Matthew B MB

Journal of insect physiology 20140606

The extent to which environmental factors influence the ability of Anopheles mosquitoes to transmit malaria parasites remains poorly explored. Environmental variation, such as change in ambient temperature, will not necessarily influence the rates of host and parasite processes equivalently, potentially resulting in complex effects on infection outcomes. As proof of principle, we used Anopheles stephensi and the rodent malaria parasite, Plasmodium yoelii, to examine the effects of a range of con ...[more]

PMID: 24911425

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Project description:Human Malaria is transmitted by mosquitoes of the genus Anopheles. Transmission is a complex phenomenon involving biological and environmental factors of humans, parasites and mosquitoes. Among more than 500 anopheline species, only a few species from different branches of the mosquito evolutionary tree transmit malaria, suggesting that their vectorial capacity has evolved independently. Anopheles albimanus (subgenus Nyssorhynchus) is an important malaria vector in the Americas. The divergence time between Anopheles gambiae, the main malaria vector in Africa, and the Neotropical vectors has been estimated to be 100 My. To better understand the biological basis of malaria transmission and to develop novel and effective means of vector control, there is a need to explore the mosquito biology beyond the An. gambiae complex.We sequenced the transcriptome of the An. albimanus adult female. By combining Sanger, 454 and Illumina sequences from cDNA libraries derived from the midgut, cuticular fat body, dorsal vessel, salivary gland and whole body, we generated a single, high-quality assembly containing 16,669 transcripts, 92% of which mapped to the An. darlingi genome and covered 90% of the core eukaryotic genome. Bidirectional comparisons between the An. gambiae, An. darlingi and An. albimanus predicted proteomes allowed the identification of 3,772 putative orthologs. More than half of the transcripts had a match to proteins in other insect vectors and had an InterPro annotation. We identified several protein families that may be relevant to the study of Plasmodium-mosquito interaction. An open source transcript annotation browser called GDAV (Genome-Delinked Annotation Viewer) was developed to facilitate public access to the data generated by this and future transcriptome projects.We have explored the adult female transcriptome of one important New World malaria vector, An. albimanus. We identified protein-coding transcripts involved in biological processes that may be relevant to the Plasmodium lifecycle and can serve as the starting point for searching targets for novel control strategies. Our data increase the available genomic information regarding An. albimanus several hundred-fold, and will facilitate molecular research in medical entomology, evolutionary biology, genomics and proteomics of anopheline mosquito vectors. The data reported in this manuscript is accessible to the community via the VectorBase website (http://www.vectorbase.org/Other/AdditionalOrganisms/).

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Dataset Information

Ambient temperature and dietary supplementation interact to shape mosquito vector competence for malaria.

Publications

Ambient temperature and dietary supplementation interact to shape mosquito vector competence for malaria.

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