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Interactions between a fungal entomopathogen and malaria parasites within a mosquito vector.

Heinig RL, Thomas MB - Malar. J. (2015)

Bottom Line: The study used two parasite species to examine possible effects of fungal infection at different parasite development stages.Similarly, for P. falciparum, there was no evidence that fungal infection affected sporozoite prevalence.These results suggest that the impact of fungus on malaria control potential is limited to the well-established effects on mosquito survival and transmission behaviour.

View Article: PubMed Central - PubMed

Affiliation: Merkle Laboratory, The Pennsylvania State University, University Park, PA, 16803, USA. yxh5118@psu.edu.

ABSTRACT

Background: Mosquitoes are becoming increasingly resistant to the chemical insecticides currently available for malaria vector control, spurring interest in alternative management tools. One promising technology is the use of fungal entomopathogens. Fungi have been shown to impact the potential for mosquitoes to transmit malaria by reducing mosquito longevity and altering behaviour associated with flight and host location. Additionally, fungi could impact the development of malaria parasites within the mosquito via competition for resources or effects on the mosquito immune system. This study evaluated whether co-infection or superinfection with the fungal entomopathogen Beauveria bassiana affected malaria infection progress in Anopheles stephensi mosquitoes.

Methods: The study used two parasite species to examine possible effects of fungal infection at different parasite development stages. First, the rodent malaria model Plasmodium yoelii was used to explore interactions at the oocyst stage. Plasmodium yoelii produces high oocyst densities in infected mosquitoes and thus was expected to maximize host immunological and resource demands. Second, fungal interactions with mature sporozoites were evaluated by infecting mosquitoes with the human malaria species Plasmodium falciparum, which is highly efficient at invading mosquito salivary glands.

Results: With P. yoelii, there was no evidence that fungal co-infection (on the same day as the blood meal) or superinfection (during a subsequent gonotrophic cycle after parasite infection) affected the proportion of mosquitoes with oocysts, the number of oocysts per infected mosquito or the number of sporozoites per oocyst. Similarly, for P. falciparum, there was no evidence that fungal infection affected sporozoite prevalence. Furthermore, there was no impact of infection with either malaria species on fungal virulence as measured by mosquito survival time.

Conclusions: These results suggest that the impact of fungus on malaria control potential is limited to the well-established effects on mosquito survival and transmission behaviour. Direct or indirect interactions between fungus and malaria parasites within mosquitoes appear to have little additional influence.

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Cumulative proportional survival of adult mosquitoes in thePlasmodium falciparumexperiment.Anopheles stephensi mosquitoes were fed on control mice, then exposed to tiles sprayed with B. bassiana conidial suspensions (‘fungus’) or blank oil (indicated by marker) either eight (d8) or 11 days later (d11, indicated by line colour). Each point represents the mean of three replicates (± standard error). (Inset) Proportional survival (y-axis) of malaria control treatments (B. bassiana fungus only and no infection groups) through day 20 following fungal exposure (x-axis).
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Fig4: Cumulative proportional survival of adult mosquitoes in thePlasmodium falciparumexperiment.Anopheles stephensi mosquitoes were fed on control mice, then exposed to tiles sprayed with B. bassiana conidial suspensions (‘fungus’) or blank oil (indicated by marker) either eight (d8) or 11 days later (d11, indicated by line colour). Each point represents the mean of three replicates (± standard error). (Inset) Proportional survival (y-axis) of malaria control treatments (B. bassiana fungus only and no infection groups) through day 20 following fungal exposure (x-axis).

Mentions: There was no evidence that mosquito survival to the infectious stage (14 days after the blood feed) was affected by P. falciparum infection (HR = 1.02, z = 0.14, p = 0.888). There was a significant interaction between fungal exposure and exposure day (HR = 5.57, z = 2.90, p = 0.004), but this was likely due to the timing of the dissections. Mosquito survival is generally quite high in the first few days of fungal infection because the fungus requires time to develop and invade the haemocoel [47]. Once the infection is established, however, mosquito survival plummets rapidly. Mosquitoes in the day 11 malaria treatments were dissected just three days after fungal exposure when very few mosquitoes had died (≤14% in all treatments, Figure 4). In contrast, mosquitoes in the day 8 treatments were dissected six days after fungal exposure, at which point mosquito mortality was much higher in the fungal treatment groups (>40%) than the controls (<10%). When only the first three days following exposure were evaluated in all the treatments, neither exposure day (HR = 0.98, z = −0.06, p = 0.95) nor fungal exposure (HR = 1.14, z = 0.34, p = 0.71 significantly influenced mortality. There was also no evidence that exposure day significantly affected mortality rate in the malaria control treatments (HR = 1.21, z = 1.79, p = 0.074), which were monitored for up to 22 days after fungal exposure (Figure 4 insert).Figure 4


Interactions between a fungal entomopathogen and malaria parasites within a mosquito vector.

Heinig RL, Thomas MB - Malar. J. (2015)

Cumulative proportional survival of adult mosquitoes in thePlasmodium falciparumexperiment.Anopheles stephensi mosquitoes were fed on control mice, then exposed to tiles sprayed with B. bassiana conidial suspensions (‘fungus’) or blank oil (indicated by marker) either eight (d8) or 11 days later (d11, indicated by line colour). Each point represents the mean of three replicates (± standard error). (Inset) Proportional survival (y-axis) of malaria control treatments (B. bassiana fungus only and no infection groups) through day 20 following fungal exposure (x-axis).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4318179&req=5

Fig4: Cumulative proportional survival of adult mosquitoes in thePlasmodium falciparumexperiment.Anopheles stephensi mosquitoes were fed on control mice, then exposed to tiles sprayed with B. bassiana conidial suspensions (‘fungus’) or blank oil (indicated by marker) either eight (d8) or 11 days later (d11, indicated by line colour). Each point represents the mean of three replicates (± standard error). (Inset) Proportional survival (y-axis) of malaria control treatments (B. bassiana fungus only and no infection groups) through day 20 following fungal exposure (x-axis).
Mentions: There was no evidence that mosquito survival to the infectious stage (14 days after the blood feed) was affected by P. falciparum infection (HR = 1.02, z = 0.14, p = 0.888). There was a significant interaction between fungal exposure and exposure day (HR = 5.57, z = 2.90, p = 0.004), but this was likely due to the timing of the dissections. Mosquito survival is generally quite high in the first few days of fungal infection because the fungus requires time to develop and invade the haemocoel [47]. Once the infection is established, however, mosquito survival plummets rapidly. Mosquitoes in the day 11 malaria treatments were dissected just three days after fungal exposure when very few mosquitoes had died (≤14% in all treatments, Figure 4). In contrast, mosquitoes in the day 8 treatments were dissected six days after fungal exposure, at which point mosquito mortality was much higher in the fungal treatment groups (>40%) than the controls (<10%). When only the first three days following exposure were evaluated in all the treatments, neither exposure day (HR = 0.98, z = −0.06, p = 0.95) nor fungal exposure (HR = 1.14, z = 0.34, p = 0.71 significantly influenced mortality. There was also no evidence that exposure day significantly affected mortality rate in the malaria control treatments (HR = 1.21, z = 1.79, p = 0.074), which were monitored for up to 22 days after fungal exposure (Figure 4 insert).Figure 4

Bottom Line: The study used two parasite species to examine possible effects of fungal infection at different parasite development stages.Similarly, for P. falciparum, there was no evidence that fungal infection affected sporozoite prevalence.These results suggest that the impact of fungus on malaria control potential is limited to the well-established effects on mosquito survival and transmission behaviour.

View Article: PubMed Central - PubMed

Affiliation: Merkle Laboratory, The Pennsylvania State University, University Park, PA, 16803, USA. yxh5118@psu.edu.

ABSTRACT

Background: Mosquitoes are becoming increasingly resistant to the chemical insecticides currently available for malaria vector control, spurring interest in alternative management tools. One promising technology is the use of fungal entomopathogens. Fungi have been shown to impact the potential for mosquitoes to transmit malaria by reducing mosquito longevity and altering behaviour associated with flight and host location. Additionally, fungi could impact the development of malaria parasites within the mosquito via competition for resources or effects on the mosquito immune system. This study evaluated whether co-infection or superinfection with the fungal entomopathogen Beauveria bassiana affected malaria infection progress in Anopheles stephensi mosquitoes.

Methods: The study used two parasite species to examine possible effects of fungal infection at different parasite development stages. First, the rodent malaria model Plasmodium yoelii was used to explore interactions at the oocyst stage. Plasmodium yoelii produces high oocyst densities in infected mosquitoes and thus was expected to maximize host immunological and resource demands. Second, fungal interactions with mature sporozoites were evaluated by infecting mosquitoes with the human malaria species Plasmodium falciparum, which is highly efficient at invading mosquito salivary glands.

Results: With P. yoelii, there was no evidence that fungal co-infection (on the same day as the blood meal) or superinfection (during a subsequent gonotrophic cycle after parasite infection) affected the proportion of mosquitoes with oocysts, the number of oocysts per infected mosquito or the number of sporozoites per oocyst. Similarly, for P. falciparum, there was no evidence that fungal infection affected sporozoite prevalence. Furthermore, there was no impact of infection with either malaria species on fungal virulence as measured by mosquito survival time.

Conclusions: These results suggest that the impact of fungus on malaria control potential is limited to the well-established effects on mosquito survival and transmission behaviour. Direct or indirect interactions between fungus and malaria parasites within mosquitoes appear to have little additional influence.

Show MeSH
Related in: MedlinePlus