Two avian Plasmodium species trigger different transcriptional responses on their vector Culex pipiens

Abstract

Malaria is a mosquito-borne disease caused by protozoans of the genus Plasmodium that affects both humans and wildlife. The fitness consequences of infections by avian malaria are well known in birds, however, little information exists on its impact on mosquitoes. Here we study how Culex pipiens mosquitoes transcriptionally respond to infection by two different Plasmodium species, P. relictum and P. cathemerium, differing in their virulence (mortality rate) and transmissibility (parasite presence in exposed mosquitoes' saliva). We studied the mosquito response to the infection at three critical stages of parasite development: the formation of ookinetes at 24 h post-infection (hpi), the release of sporozoites into the hemocoel at 10 days post-infection (dpi), and the storage of sporozoites in the salivary glands at 21 dpi. For each time point, we characterized the gene expression of mosquitoes infected with each P. relictum and P. cathemerium and mosquitoes fed on an uninfected bird and, subsequently, compared their transcriptomic responses. Differential gene expression analysis showed that most transcriptomic changes occurred during the early infection stage (24 hpi), especially when comparing P. relictum and P. cathemerium-infected mosquitoes. Differentially expressed genes in mosquitoes infected with each species were related mainly to the metabolism of the immune response, trypsin, and other serine-proteases. We conclude that these differences in response may partly play a role in the differential virulence and transmissibility previously observed between P. relictum and P. cathemerium in Cx. pipiens.