Limits...
A possible mechanism for the suppression of Plasmodium berghei development in the mosquito Anopheles gambiae by the microsporidian Vavraia culicis.

Bargielowski I, Koella JC - PLoS ONE (2009)

Bottom Line: We evaluated the possibility that larval infection by a microsporidian primes the immune system of adult mosquitoes in a way that enables a more effective anti-Plasmodium response.To do so, we infected 2-day old larvae of the mosquito Anopheles gambiae with one of 4 isolates of the microsporidian Vavraia culicis and reared one group as an uninfected control.Within each treatment, we fed half the adult females on a mix of P. berghei ookinetes and blood and inoculated the other half with a negatively charged CM-25 Sephadex bead to evaluate the mosquitoes' melanisation response.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, Faculty of Natural Sciences, Imperial College London, London, United Kingdom. irka.bargielowski06@imperial.ac.uk

ABSTRACT

Background: Microsporidian parasites of mosquitoes offer a possible way of controlling malaria, as they impede the development of Plasmodium parasites within the mosquito. The mechanism involved in this interference process is unknown.

Methodology: We evaluated the possibility that larval infection by a microsporidian primes the immune system of adult mosquitoes in a way that enables a more effective anti-Plasmodium response. To do so, we infected 2-day old larvae of the mosquito Anopheles gambiae with one of 4 isolates of the microsporidian Vavraia culicis and reared one group as an uninfected control. Within each treatment, we fed half the adult females on a mix of P. berghei ookinetes and blood and inoculated the other half with a negatively charged CM-25 Sephadex bead to evaluate the mosquitoes' melanisation response.

Conclusions: The microsporidian-infected mosquitoes were less likely to harbour oocysts (58.5% vs. 81.8%), harboured fewer oocysts (8.9 oocysts vs. 20.7 oocysts) if the malaria parasite did develop and melanised the Sephadex bead to a greater degree (73% vs. 35%) than the controls. While the isolates differed in the number of oocysts and in the melanisation response, the stimulation of the immune response was not correlated with either measure of malaria development. Nevertheless, the consistent difference between microsporidian-infected and -uninfected mosquitoes--more effective melanisation and less successful infection by malaria--suggests that microsporidians impede the development of malaria by priming the mosquito's immune system.

Show MeSH

Related in: MedlinePlus

Success of infection by P. berghei in control mosquitoes and mosquitoes infected by one of four isolates of V. culicis.(a) The proportion of mosquitoes that harboured at least one oocyst 10 days after blood feeding. (b) The mean number of oocysts in mosquitoes with at least one oocyst. In both panels, the vertical lines show the standard errors of the estimates, the horizontal, dotted lines show the means of the controls, and the numbers in the bars indicate the number of mosquitoes analyzed. The isolates are numbered in order of increasing melanisation efficacy (see Figure 2).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2651578&req=5

pone-0004676-g001: Success of infection by P. berghei in control mosquitoes and mosquitoes infected by one of four isolates of V. culicis.(a) The proportion of mosquitoes that harboured at least one oocyst 10 days after blood feeding. (b) The mean number of oocysts in mosquitoes with at least one oocyst. In both panels, the vertical lines show the standard errors of the estimates, the horizontal, dotted lines show the means of the controls, and the numbers in the bars indicate the number of mosquitoes analyzed. The isolates are numbered in order of increasing melanisation efficacy (see Figure 2).

Mentions: Of the 159 adult females exposed to the Plasmodium-infected blood meal, 119 (75%) took a full blood meal and survived the 10 days up to being dissected. There was no difference in feeding success between uninfected control mosquitoes (75.4%) and microsporidian-infected mosquitoes (74%) (χ2 = 0.03, p = 0.860), but the proportion of mosquitoes that fed did depend on the microsporidian isolate that infected them (χ2 = 7.55, p = 0.056), ranging from 64% to 87%. Of the 116 fed mosquitoes, 73 harboured oocysts 10 days later. Blocking had no effect on the feeding efficiency of the mosquitoes, except for treatment with isolate 3, where more mosquitoes from block one took a blood meal than block two (χ2 = 6.046, p = 0.0139). Microsporidian-infected mosquitoes were less likely (58.5%) to harbour oocysts than microsporidian-uninfected controls (81.8%) (χ2 = 4.40, p = 0.036) (Fig. 1a). The effect of the microsporidian isolate on the proportion of mosquitoes with oocysts ranged from 54.5% to 65.2%, but this difference was far from statistically significant (χ2 = 0.65, p = 0.885). The mean number of oocysts in the 73 mosquitoes with at least 1 oocyst was 11.9, ranging from 4.8 to 20.7 among the five treatments (Fig. 1b; analysis of square root of oocyst number: F5,67 = 7.82, p<0.001). Block had no effect on the number of oocysts harboured by mosquitoes in each treatment group. Mosquitoes infected by a microsporidian harboured an average of 8.9 oocysts; controls harboured 20.7 oocysts (F1,69 = 30.93, p<0.001). The mean number of oocysts in mosquitoes infected by different microsporidian isolates ranged from 4.8 to 13.8 (F1,47 = 5.45, p = 0.003).


A possible mechanism for the suppression of Plasmodium berghei development in the mosquito Anopheles gambiae by the microsporidian Vavraia culicis.

Bargielowski I, Koella JC - PLoS ONE (2009)

Success of infection by P. berghei in control mosquitoes and mosquitoes infected by one of four isolates of V. culicis.(a) The proportion of mosquitoes that harboured at least one oocyst 10 days after blood feeding. (b) The mean number of oocysts in mosquitoes with at least one oocyst. In both panels, the vertical lines show the standard errors of the estimates, the horizontal, dotted lines show the means of the controls, and the numbers in the bars indicate the number of mosquitoes analyzed. The isolates are numbered in order of increasing melanisation efficacy (see Figure 2).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2651578&req=5

pone-0004676-g001: Success of infection by P. berghei in control mosquitoes and mosquitoes infected by one of four isolates of V. culicis.(a) The proportion of mosquitoes that harboured at least one oocyst 10 days after blood feeding. (b) The mean number of oocysts in mosquitoes with at least one oocyst. In both panels, the vertical lines show the standard errors of the estimates, the horizontal, dotted lines show the means of the controls, and the numbers in the bars indicate the number of mosquitoes analyzed. The isolates are numbered in order of increasing melanisation efficacy (see Figure 2).
Mentions: Of the 159 adult females exposed to the Plasmodium-infected blood meal, 119 (75%) took a full blood meal and survived the 10 days up to being dissected. There was no difference in feeding success between uninfected control mosquitoes (75.4%) and microsporidian-infected mosquitoes (74%) (χ2 = 0.03, p = 0.860), but the proportion of mosquitoes that fed did depend on the microsporidian isolate that infected them (χ2 = 7.55, p = 0.056), ranging from 64% to 87%. Of the 116 fed mosquitoes, 73 harboured oocysts 10 days later. Blocking had no effect on the feeding efficiency of the mosquitoes, except for treatment with isolate 3, where more mosquitoes from block one took a blood meal than block two (χ2 = 6.046, p = 0.0139). Microsporidian-infected mosquitoes were less likely (58.5%) to harbour oocysts than microsporidian-uninfected controls (81.8%) (χ2 = 4.40, p = 0.036) (Fig. 1a). The effect of the microsporidian isolate on the proportion of mosquitoes with oocysts ranged from 54.5% to 65.2%, but this difference was far from statistically significant (χ2 = 0.65, p = 0.885). The mean number of oocysts in the 73 mosquitoes with at least 1 oocyst was 11.9, ranging from 4.8 to 20.7 among the five treatments (Fig. 1b; analysis of square root of oocyst number: F5,67 = 7.82, p<0.001). Block had no effect on the number of oocysts harboured by mosquitoes in each treatment group. Mosquitoes infected by a microsporidian harboured an average of 8.9 oocysts; controls harboured 20.7 oocysts (F1,69 = 30.93, p<0.001). The mean number of oocysts in mosquitoes infected by different microsporidian isolates ranged from 4.8 to 13.8 (F1,47 = 5.45, p = 0.003).

Bottom Line: We evaluated the possibility that larval infection by a microsporidian primes the immune system of adult mosquitoes in a way that enables a more effective anti-Plasmodium response.To do so, we infected 2-day old larvae of the mosquito Anopheles gambiae with one of 4 isolates of the microsporidian Vavraia culicis and reared one group as an uninfected control.Within each treatment, we fed half the adult females on a mix of P. berghei ookinetes and blood and inoculated the other half with a negatively charged CM-25 Sephadex bead to evaluate the mosquitoes' melanisation response.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, Faculty of Natural Sciences, Imperial College London, London, United Kingdom. irka.bargielowski06@imperial.ac.uk

ABSTRACT

Background: Microsporidian parasites of mosquitoes offer a possible way of controlling malaria, as they impede the development of Plasmodium parasites within the mosquito. The mechanism involved in this interference process is unknown.

Methodology: We evaluated the possibility that larval infection by a microsporidian primes the immune system of adult mosquitoes in a way that enables a more effective anti-Plasmodium response. To do so, we infected 2-day old larvae of the mosquito Anopheles gambiae with one of 4 isolates of the microsporidian Vavraia culicis and reared one group as an uninfected control. Within each treatment, we fed half the adult females on a mix of P. berghei ookinetes and blood and inoculated the other half with a negatively charged CM-25 Sephadex bead to evaluate the mosquitoes' melanisation response.

Conclusions: The microsporidian-infected mosquitoes were less likely to harbour oocysts (58.5% vs. 81.8%), harboured fewer oocysts (8.9 oocysts vs. 20.7 oocysts) if the malaria parasite did develop and melanised the Sephadex bead to a greater degree (73% vs. 35%) than the controls. While the isolates differed in the number of oocysts and in the melanisation response, the stimulation of the immune response was not correlated with either measure of malaria development. Nevertheless, the consistent difference between microsporidian-infected and -uninfected mosquitoes--more effective melanisation and less successful infection by malaria--suggests that microsporidians impede the development of malaria by priming the mosquito's immune system.

Show MeSH
Related in: MedlinePlus