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Malaria parasite immune evasion and adaptation to its mosquito host is influenced by the acquisition of multiple blood meals

View ORCID ProfileHyeogsun Kwon, Rebekah A. Reynolds, Maria L. Simões, View ORCID ProfileGeorge Dimopoulos, View ORCID ProfileRyan C. Smith
doi: https://doi.org/10.1101/801480
Hyeogsun Kwon
1Department of Entomology, Iowa State University, Ames, Iowa, USA
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Rebekah A. Reynolds
1Department of Entomology, Iowa State University, Ames, Iowa, USA
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Maria L. Simões
2Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA
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George Dimopoulos
2Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA
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Ryan C. Smith
1Department of Entomology, Iowa State University, Ames, Iowa, USA
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  • For correspondence: smithr@iastate.edu
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Abstract

A minimum of two blood meals are required for a mosquito to acquire and transmit malaria, yet Anopheles mosquitoes frequently obtain additional blood meals during their adult lifespan. To determine the impact of subsequent blood-feeding on parasite development in Anopheles gambiae, we examined rodent and human Plasmodium parasite infection with or without an additional non-infected blood meal. We find that an additional blood meal significantly reduces P. berghei immature oocyst numbers, yet does not influence mature oocysts that have already begun sporogony. This is in contrast to experiments performed with the human parasite, P. falciparum, where an additional blood meal does not affect oocyst numbers. These observations are reproduced when mosquitoes were similarly challenged with an artificial protein meal, suggesting that parasite losses are due to the physical distension of the mosquito midgut. We provide evidence that feeding compromises the integrity of the midgut basal lamina, enabling the recognition and lysis of immature P. berghei oocysts by the mosquito complement system. Moreover, we demonstrate that additional feeding promotes P. falciparum oocyst growth, suggesting that human malaria parasites exploit host resources provided with blood-feeding to accelerate their growth. This contrasts experiments with P. berghei, where the size of surviving oocysts is independent of an additional blood meal. Together, these data demonstrate differences in the ability of Plasmodium species to evade immune detection and adapt to utilize host resources at the oocyst stage, representing an additional, yet unexplored component of vectorial capacity that has important implications for transmission of malaria.

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Posted October 15, 2019.
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Malaria parasite immune evasion and adaptation to its mosquito host is influenced by the acquisition of multiple blood meals
Hyeogsun Kwon, Rebekah A. Reynolds, Maria L. Simões, George Dimopoulos, Ryan C. Smith
bioRxiv 801480; doi: https://doi.org/10.1101/801480
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Malaria parasite immune evasion and adaptation to its mosquito host is influenced by the acquisition of multiple blood meals
Hyeogsun Kwon, Rebekah A. Reynolds, Maria L. Simões, George Dimopoulos, Ryan C. Smith
bioRxiv 801480; doi: https://doi.org/10.1101/801480

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