Abstract
Animal and human pathogens that are transmitted by arthropods are a global concern, particularly those vectored by mosquitoes (e.g., Plasmodium spp. and dengue virus). Vector microbiota may hold the key to vector-borne pathogen control, as mounting evidence suggests that the contributions of the vector microbiota to vector physiology and pathogen life cycle are so relevant that vectorial capacity cannot be understood without considering microbial communities within the vectors. Anti-tick microbiota vaccines targeting commensal bacteria of the vector microbiota alter vector feeding and modulate the taxonomic and functional profiles of vector microbiome, but their impact on vector-borne pathogen development within the vector has not been tested. In this study, we tested whether anti-microbiota vaccination in birds targeting Enterobacteriaceae within mosquito midguts modulates the mosquito microbiota and disrupt Plasmodium relictum development in its natural vector Culex quinquefasciatus. Domestic canaries (Serinus canaria domestica) were experimentally infected with P. relictum and/or immunized with live vaccines containing different strains of Escherichia coli. Immunization of birds induced E. coli-specific antibodies. The midgut microbial communities of mosquitoes fed on Plasmodium-infected and/or E. coli-immunized birds were different from those of mosquitoes fed on control birds. Notably, mosquito midgut microbiota modulation was associated with a significant decrease in the occurrence of P. relictum oocysts and sporozoites in the midguts and salivary glands of C. quinquefasciatus, respectively. A significant reduction in the number of oocysts was also observed. These findings suggest that anti-microbiota vaccines can be used as a novel tool to control malaria transmission and potentially other vector-borne pathogens.
Highlights
IntroductionMosquitoes are vectors of major human diseases such as dengue (caused by dengue virus), and malaria (caused by Plasmodium spp.) [1]
Mosquitoes are vectors of major human diseases such as dengue, and malaria [1]
No significant change was observed in the levels of anti-E. coli Abs in birds that received the mock vaccination (PBS) or those only infected with Plasmodium (Figure 2A)
Summary
Mosquitoes are vectors of major human diseases such as dengue (caused by dengue virus), and malaria (caused by Plasmodium spp.) [1]. The parasite traverses the peritrophic membrane and epithelial layer of the midgut and develops to oocysts [3]. Of special interest are the interactions between the vector, its microbiota and transmitted pathogens, since commensal bacteria interact with mosquito-borne pathogens [9] and can facilitate [10] or compete [11] with pathogen colonization and development within the vector midguts, prompting research into microbiota manipulation and transmission-blocking strategies [12]. Depleting vector microbiota from bacteria that facilitates pathogen development could be exploited as a mean for blocking transmission. The bacterium Asaia bogorensis increases midgut pH promoting Plasmodium berghei gametogenesis within Anopheles stephensi [10], and high abundance of Enterobacteriaceae increases Plasmodium falciparum infection in Anopheles gambiae midgut [13], making the reduction of these bacterial species a sound strategy to reduce pathogen infection in the vector and potentially block transmission to the host
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