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The Impact of Temperature on the Sporogonic Development of the Tropical Avian Malaria Parasite Plasmodium relictum (Genetic Lineage pGRW4) in Culex pipiens Form molestus Mosquitoes.

ABSTRACT: The avian malaria parasite Plasmodium relictum (genetic lineage pGRW4) is known to cause severe pathology in nonadapted vertebrate hosts. This parasite is prevalent in some bird species in Northern Europe, however the records obtained are only from adult long-distance migrant birds after their return from the wintering grounds. A recent experimental study showed that this parasite completes sporogonic development in the local European vector Culex pipiens at a controlled mean temperature of 19 °C. Thereby, temperature limits for the transmission of this parasite in Northern Europe remain unknown. In this study, we took a step further and tested the impact of different temperature conditions, including some extreme fluctuations between 23 °C down to 7 °C, on the sporogonic development of P. relictum (pGRW4) in the vector Culex pipiens form molestus. Mosquitoes were exposed to infection and kept under different air-temperature conditions: (i) constant warm temperature, (ii) natural outdoor temperatures and (iii) temporary exposure to low temperatures. Plasmodium relictum (pGRW4) completed sporogony in mosquitoes of all experimental groups, however different patterns of the sporogonic development depending on temperature conditions were observed. Based on these results, we conclude that the cool air temperature of Northern Europe in summer is not a limiting factor in successful development of the parasite. However, delayed sporogony caused by low summer temperatures may have a detrimental impact on the active transmission of this parasite in Northern Europe.

SUBMITTER: Platonova E

PROVIDER: S-EPMC8620208 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundPlasmodium parasites that cause bird malaria occur in all continents except Antarctica and are primarily transmitted by mosquitoes in the genus Culex. Culex quinquefasciatus, the mosquito vector of avian malaria in Hawai'i, became established in the islands in the 1820s. While the deadly effects of malaria on endemic bird species have been documented for many decades, vector-parasite interactions in avian malaria systems are relatively understudied.MethodsTo evaluate the gene expression response of mosquitoes exposed to a Plasmodium infection intensity known to occur naturally in Hawai'i, offspring of wild-collected Hawaiian Cx. quinquefasciatus were fed on a domestic canary infected with a fresh isolate of Plasmodium relictum GRW4 from a wild-caught Hawaiian honeycreeper. Control mosquitoes were fed on an uninfected canary. Transcriptomes of five infected and three uninfected individual mosquitoes were sequenced at each of three stages of the parasite life cycle: 24 h post feeding (hpf) during ookinete invasion; 5 days post feeding (dpf) when oocysts are developing; 10 dpf when sporozoites are released and invade the salivary glands.ResultsDifferential gene expression analyses showed that during ookinete invasion (24 hpf), genes related to oxidoreductase activity and galactose catabolism had lower expression levels in infected mosquitoes compared to controls. Oocyst development (5 dpf) was associated with reduced expression of a gene with a predicted innate immune function. At 10 dpf, infected mosquitoes had reduced expression levels of a serine protease inhibitor, and further studies should assess its role as a Plasmodium agonist in C. quinquefasciatus. Overall, the differential gene expression response of Hawaiian Culex exposed to a Plasmodium infection intensity known to occur naturally in Hawai'i was low, but more pronounced during ookinete invasion.ConclusionsThis is the first analysis of the transcriptional responses of vectors to malaria parasites in non-mammalian systems. Interestingly, few similarities were found between the response of Culex infected with a bird Plasmodium and those reported in Anopheles infected with human Plasmodium. The relatively small transcriptional changes observed in mosquito genes related to immune response and nutrient metabolism support conclusions of low fitness costs often documented in experimental challenges of Culex with avian Plasmodium.

Project description:BACKGROUND: The control of most vectors of malaria is threatened by the spread of insecticide resistance. One factor that has been hitherto largely overlooked is the potential effects of insecticide resistance on the ability of mosquitoes to transmit malaria: are insecticide-resistant mosquitoes as good vectors of Plasmodium as susceptible ones? The drastic physiological changes that accompany the evolution of insecticide resistance may indeed alter the ability of vectors to transmit diseases, a possibility that, if confirmed, could have major epidemiological consequences. METHODS: Using a novel experimental system consisting of the avian malaria parasite (Plasmodium relictum) and its natural vector (the mosquito Culex pipiens), two of the most common mechanisms of insecticide resistance (esterase overproduction and acetylcholinesterase modification) were investigated for their effect on mosquito infection rate and parasite burden. For this purpose two types of experiments were carried out using (i) insecticide-resistant and susceptible laboratory isogenic lines of Cx. pipiens and (ii) wild Cx. pipiens collected from a population where insecticide resistant and susceptible mosquitoes coexist in sympatry. RESULTS: The isogenic line and wild-caught mosquito experiments were highly consistent in showing no effect of either esterase overproduction or of acetylcholinesterase modification on either the infection rate or on the oocyst burden of mosquitoes. The only determinant of these traits was blood meal size, which was similar across the different insecticide resistant categories in both experiments. CONCLUSIONS: Insecticide resistance was found to have no effect on Plasmodium development within the mosquito. This is the first time this question has been addressed using a natural mosquito-Plasmodium combination, while taking care to standardize the genetic background against which the insecticide resistance genes operate. Infection rate and oocyst burden are but two of the factors that determine the vectorial capacity of mosquitoes. Other key determinants of parasite transmission, such as mosquito longevity and behaviour, or the parasite's incubation time, need to be investigated before concluding on whether insecticide resistance influences the ability of mosquitoes to transmit malaria.

Dataset Information

The Impact of Temperature on the Sporogonic Development of the Tropical Avian Malaria Parasite Plasmodium relictum (Genetic Lineage pGRW4) in Culex pipiens Form molestus Mosquitoes.

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