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

2019 ◽  
Author(s):  
Hyeogsun Kwon ◽  
Rebekah A. Reynolds ◽  
Maria L. Simões ◽  
George Dimopoulos ◽  
Ryan C. Smith

AbstractA 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.

mSphere ◽  
2021 ◽  
Vol 6 (2) ◽  
Author(s):  
Hyeogsun Kwon ◽  
Maria L. Simões ◽  
Rebekah A. Reynolds ◽  
George Dimopoulos ◽  
Ryan C. Smith

ABSTRACT Mosquitoes may feed multiple times during their life span in addition to those times needed to acquire and transmit malaria. To determine the impact of subsequent blood feeding on parasite development in Anopheles gambiae, we examined Plasmodium parasite infection with or without an additional noninfected blood meal. We found that an additional blood meal significantly reduced Plasmodium berghei immature oocyst numbers, yet had no effect on the human parasite Plasmodium falciparum. These observations were reproduced when mosquitoes were fed an artificial protein meal, suggesting that parasite losses are independent of blood ingestion. We found that feeding with either a blood or protein meal compromises midgut basal lamina integrity as a result of the physical distention of the midgut, enabling the recognition and lysis of immature P. berghei oocysts by mosquito complement. 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 is in contrast to experiments with P. berghei, where the size of surviving oocysts is independent of an additional blood meal. Together, these data demonstrate distinct differences in Plasmodium species in evading immune detection and utilizing host resources at the oocyst stage, representing an additional, yet unexplored component of vectorial capacity that has important implications for the transmission of malaria. IMPORTANCE Mosquitoes must blood feed multiple times to acquire and transmit malaria. However, the impact of an additional mosquito blood meal following malaria parasite infection has not been closely examined. Here, we demonstrate that additional feeding affects mosquito vector competence; namely, additional feeding significantly limits Plasmodium berghei infection, yet has no effect on infection of the human parasite P. falciparum. Our experiments support that these killing responses are mediated by the physical distension of the midgut and by temporary damage to the midgut basal lamina that exposes immature P. berghei oocysts to mosquito complement, while human malaria parasites are able to evade these killing mechanisms. In addition, we provide evidence that additional feeding promotes P. falciparum oocyst growth. This is in contrast to P. berghei, where oocyst size is independent of an additional blood meal. This suggests that human malaria parasites are able to exploit host resources provided by an additional feeding to accelerate their growth. In summary, our data highlight distinct differences in malaria parasite species in evading immune recognition and adapting to mosquito blood feeding. These observations have important, yet previously unexplored, implications for the impact of multiple blood meals on the transmission of malaria.


2018 ◽  
Author(s):  
James Orsborne ◽  
Luis Furuya-Kanamori ◽  
Claire L. Jeffries ◽  
Mojca Kristan ◽  
Abdul Rahim Mohammed ◽  
...  

AbstractDifficulties with observing the dispersal of insect vectors in the field have hampered understanding of several aspects of their behaviour linked to disease transmission. Here, a novel method based on detection of blood-meal sources is introduced to inform two critical and understudied mosquito behaviours: plasticity in the malaria vector’s blood-host choice and vector dispersal. Strategically located collections of Anopheles coluzzii from a malaria-endemic village of southern Ghana showed statistically significant variation in host species composition of mosquito blood-meals. Trialling a new sampling approach gave the first estimates for the remarkably local spatial scale across which host choice is plastic. Using quantitative PCR, the blood-meal digestion was then quantified for field-caught mosquitoes and calibrated according to timed blood digestion in colony mosquitoes. We demonstrate how this new ‘molecular Sella score’ approach can be used to estimate the dispersal rate of blood-feeding vectors caught in the field.


2021 ◽  
Author(s):  
Rex B Mbewe ◽  
John Keven ◽  
Themba Mzilahowa ◽  
Lauren Cohee ◽  
Miriam K Laufer ◽  
...  

Abstract BackgroundSelection of blood meal hosts by mosquitoes is a key variable in the vectorial capacity of Anopheles mosquitoes for human malaria. Blood feeding on humans is likely to be modulated by use of different types of long-lasting insecticidal nets (LLINs) and the effectiveness of LLINs is impacted by the relative intensity of insecticide resistance. The aim of this study was to test the hypothesis that LLINs containing pyrethroid and the synergist piperonyl butoxide (PBO) would lead to a reduction of human host utilization than LLINs containing only pyrethroid and that blood feeding patterns of Anopheles in Malawi compromise malaria interventions.MethodsFemale Anopheles mosquitoes were sampled indoors from May 2019 through April 2020 by aspiration, pyrethrum spray catch, and CDC light trap in rural villages of Namanolo (conventional nets) and Ntaja (PBO nets) in Balaka and Machinga districts respectively. Anopheles species, blood meal sources, and infection with Plasmodium falciparum in the head and thorax of individual mosquitoes were determined with PCR.ResultsOf a total of 6,585 Anopheles females sampled indoors in 203 houses, 633 (9.6%) were blood-fed and consisted of An. arabiensis (44.1% (n = 279)), An. gambiae s.s (16.2% (n = 103)), An. funestus s.s (33.5% (n = 212)), An. parensis 0.3% (n = 2), and unidentified Anopheles spp (5.8% (n = 37)). Of the 541 mosquitoes (85.5%) successfully identified blood meals, 436 (81.0%) were solely human, 28 (5.2%) goat, 11 (2.0%) dog, 60 (11.1%) mixed goat-human, 5 (0.9%) dog-human, and 1 dog-goat. Human blood index and EIR was high in Namanolo than Ntaja (0.96 vs 0.89 (p = 0.001) and 0.11 vs 0.06 infective bites per person per year respectively) despite high net ownership (92%) and nightly use (75%) rates. Relative to host availability, non-human hosts were over selected in the two sites.ConclusionThe use of PBO nets was associated with lower HBI and EIR, however, the wide availability of LLINs was still associated with extensive successful human blood meals by the main malaria vectors in Malawi. The presence of a small fraction of mixed blood meals indicates constrained plasticity of Anopheles vectors to switch to non-human hosts and circumvent malaria control interventions.


1990 ◽  
Vol 25 (1) ◽  
pp. 57-63
Author(s):  
Adel S. El-Akad ◽  
J. G. Humphreys

Field observations and laboratory studies were conducted to determine the effects of a pre-mating blood meal on mating, ovarian development and oviposition in Anopheles pharoensis (Theobald). Approximately 24% of the females blood feed before mating; however, swollen abdomens of blood-fed females interfere with the mating process. In females which mated prior to first blood meal, first oviposition occurred at 6.6 days and required only a single blood meal. A second blood meal takes them to the second oviposition in an additional 2.5 days; the third oviposition required 1.4 blood meals and occurred 3 days after the second oviposition. Blood-fed unmated females reach first oviposition at 13.4 days and require an average of 4 blood meals prior to the first oviposition. At this age, the female is chronologically old and even if mating now occurs, egg production is greatly reduced and continues to decrease through subsequent ovipositions until death. The taking of a blood meal prior to mating greatly decreases the reproductive potential of this species.


Genes ◽  
2019 ◽  
Vol 10 (3) ◽  
pp. 211 ◽  
Author(s):  
Emmanuel Elanga-Ndille ◽  
Lynda Nouage ◽  
Achille Binyang ◽  
Tatiane Assatse ◽  
Billy Tene-Fossog ◽  
...  

D7 family proteins are among the most expressed salivary proteins in mosquitoes. They facilitate blood meal intake of the mosquito by scavenging host amines that induce vasoconstriction, platelet aggregation and pain. Despite this important role, little information is available on the impact of insecticide resistance on the regulation of D7 proteins and consequently on the blood feeding success. In this study, real-time quantitative polymerase chain reaction (qPCR) analyses were performed to investigate how pyrethroid resistance could influence the expression of genes encoding D7 family proteins in Anopheles gambiae and Anopheles funestus s.s. mosquitoes from Elon in the Central Cameroon. Out of 328 collected mosquitoes, 256 were identified as An. funestus sl and 64 as An. gambiae sl. Within the An. funestus group, An. funestus s.s. was the most abundant species (95.95%) with An. rivulorum, An. parensis and An. rivulorum-like also detected. All An. gambiae s.l mosquitoes were identified as An. gambiae. High levels of pyrethroid resistance were observed in both An. gambiae and An. funestus mosquitoes. RT-qPCR analyses revealed a significant overexpression of two genes encoding D7 proteins, D7r3 and D7r4, in pyrethroids resistant An. funestus. However, no association was observed between the polymorphism of these genes and their overexpression. In contrast, overall D7 salivary genes were under-expressed in pyrethroid resistant An. gambiae. This study provides preliminary evidences that pyrethroid resistance could influence blood meal intake through over-expression of D7 proteins although future studies will help establishing potential impact on vectorial capacity.


2018 ◽  
Vol 2018 ◽  
pp. 1-10 ◽  
Author(s):  
C. S. Moraes ◽  
K. Aguiar-Martins ◽  
S. G. Costa ◽  
P. A. Bates ◽  
R. J. Dillon ◽  
...  

Lutzomyia longipalpis is the main vector of visceral leishmaniasis (VL) in America. Physiological and molecular mechanisms of Leishmania infection in sand flies have been studied during the first gonotrophic cycle. There are few studies about these interactions during the second gonotrophic cycle mainly because of the difficulties maintaining sand flies through sequential feeds. Here we standardized conditions to perform the second blood feed efficiently, and our results show that oviposition is an essential factor for the success of multiple feeds. We evaluated the impact of the second blood meal on longevity, protein digestion, trypsin activity, and Leishmania mexicana development within L. longipalpis gut. Mortality of blood-fed females increases after second blood meal as compared to sugar-fed females. Trypsin activity was lower during the second gonotrophic cycle. However, no difference in protein intake was observed between blood meals. There was no difference in the population size of Leishmania in the gut after both blood meals. In this work, we presented an optimized protocol for obtaining sufficient numbers of sand fly females fed on a second blood meal, and we described some physiological and parasitological aspects of the second gonotrophic cycle which might influence the vectorial competence of sand flies.


2021 ◽  
Vol 15 (9) ◽  
pp. e0009815
Author(s):  
Garrett P. League ◽  
Ethan C. Degner ◽  
Sylvie A. Pitcher ◽  
Yassi Hafezi ◽  
Erica Tennant ◽  
...  

Background Aedes aegypti mosquitoes are globally distributed vectors of viruses that impact the health of hundreds of millions of people annually. Mating and blood feeding represent fundamental aspects of mosquito life history that carry important implications for vectorial capacity and for control strategies. Females transmit pathogens to vertebrate hosts and obtain essential nutrients for eggs during blood feeding. Further, because host-seeking Ae. aegypti females mate with males swarming near hosts, biological crosstalk between these behaviors could be important. Although mating influences nutritional intake in other insects, prior studies examining mating effects on mosquito blood feeding have yielded conflicting results. Methodology/Principal findings To resolve these discrepancies, we examined blood-feeding physiology and behavior in virgin and mated females and in virgins injected with male accessory gland extracts (MAG), which induce post-mating changes in female behavior. We controlled adult nutritional status prior to blood feeding by using water- and sugar-fed controls. Our data show that neither mating nor injection with MAG affect Ae. aegypti blood intake, digestion, or feeding avidity for an initial blood meal. However, sugar feeding, a common supplement in laboratory settings but relatively rare in nature, significantly affected all aspects of feeding and may have contributed to conflicting results among previous studies. Further, mating, MAG injection, and sugar intake induced declines in subsequent feedings after an initial blood meal, correlating with egg production and laying. Taking our evaluation to the field, virgin and mated mosquitoes collected in Colombia were equally likely to contain blood at the time of collection. Conclusions/Significance Mating, MAG, and sugar feeding impact a mosquito’s estimated ability to transmit pathogens through both direct and indirect effects on multiple aspects of mosquito biology. Our results highlight the need to consider natural mosquito ecology, including diet, when assessing their physiology and behavior in the laboratory.


2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Ephantus J. Muturi ◽  
Teresia M. Njoroge ◽  
Christopher Dunlap ◽  
Carla E. Cáceres

Abstract Background The guts of blood-sucking insects host a community of bacteria that can shift dramatically in response to biotic and abiotic factors. Identifying the key factors structuring these microbial communities has important ecological and epidemiological implications. Methods We used the yellow fever mosquito, Aedes aegypti, to investigate the impact of mixed blood meals on gut microbiota of vector mosquitoes. Adult females were experimentally fed on sugar or blood from chicken, rabbit or a mixture of chicken and rabbit blood, and their gut microbiota were characterized using 16S rRNA gene amplification and MiSeq sequencing. Results The gut bacterial communities of mosquitoes fed on the three blood meal treatments clustered separately, suggesting that host species identity and mixed blood-feeding are key determinants of gut bacterial community composition in mosquitoes. Mixed blood meal had a synergistic effect on both operational taxonomic unit (OTU) richness and the Shannon diversity index, suggesting that mixed blood-feeding can offset the nutritional deficit of blood meals from certain host species. The microbial communities observed in this study were distinct from those identified from similarly fed Ae. aegypti from our previous study. Conclusions These findings demonstrate that vector host-feeding preferences can influence gut microbial composition and diversity, which could potentially impact pathogen acquisition and transmission by the vector. The results also demonstrate that different microenvironmental conditions within the laboratory may play an important role in structuring the microbial communities of independently reared mosquito colonies.


1983 ◽  
Vol 78 (1) ◽  
pp. 37-47 ◽  
Author(s):  
Rotraut A. G. B. Cônsoli ◽  
Paul Williams ◽  
Elizabeth C. Moreno ◽  
Bernadete S. Santos

Observations were made on 100 female Aedes fluviatilis (Lutz) maintained individually from the first blood meal onwards and allowed one blood meal during each oviposition cycle, 5% dextrose solution been supplied throughout life. The average length of live was 49.9 ± 17.8 days; the logarithm of the mortality rate increased proportionately to physiological age. The insects took an average of 7.3 ± 3.2 blood meals and produced a mean of 7.9 ± 3.7 clutches of eggs. There was a progressive decrease, proportional to advancing physiological age, in the mean numbers of eggs laid in successive oviposition cycles, in the intervals between blood feeding oviposition, and in the numbers of larvae that hatched. Delayed oviposition, transient sterility and a total loss of fertility were also recorded.


2021 ◽  
Vol 15 (8) ◽  
pp. e0009682
Author(s):  
Martin J. R. Hall ◽  
Debashis Ghosh ◽  
Daniel Martín-Vega ◽  
Brett Clark ◽  
Innes Clatworthy ◽  
...  

Leishmaniasis is a debilitating disease of the tropics, subtropics and southern Europe caused by Leishmania parasites that are transmitted during blood feeding by phlebotomine sand flies (Diptera: Psychodidae). Using non-invasive micro-computed tomography, we were able to visualize the impact of the laboratory model infection of Lutzomyia longipalpis with Leishmania mexicana and its response to a second blood meal. For the first time we were able to show in 3D the plug of promastigote secretory gel (PSG) and parasites in the distended midgut of whole infected sand flies and measure its volume in relation to that of the midgut. We were also able to measure the degree of opening of the stomodeal valve and demonstrate the extension of the PSG and parasites into the pharynx. Although our pilot study could only examine a few flies, it supports the hypothesis that a second, non-infected, blood meal enhances parasite transmission as we showed that the thoracic PSG-parasite plug in infected flies after a second blood meal was, on average, more than twice the volume of the plug in infected flies that did not have a second blood meal.


Sign in / Sign up

Export Citation Format

Share Document