Anti-Microbiota Vaccine Reduces Avian Malaria Infection Within Mosquito Vectors

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.

Rickettsial pathogens drive microbiota assembly in Hyalomma marginatum and Rhipicephalus bursa ticks

“…Reducing network robustness by anti‐microbiota vaccines presents a novel strategy to impact vector microbiota, as demonstrated by Mateos‐Hernández et al (2021). This approach aims to induce infection‐refractory states in ticks or other vectors, as highlighted by Maitre, Wu‐Chuang, Aželytė, et al (2022) and Maitre, Wu‐Chuang, Mateos‐Hernández, et al (2022), ultimately leading to a reduction or blockade of vector‐borne pathogen transmission (Aželytė et al, 2022). Previous research showed that anti‐microbiota vaccines that targets keystone taxa can modulate the tick microbiota (Mateos‐Hernández et al, 2020, 2021).…”

Comparison of salivary gland and midgut microbiome in the soft ticks Ornithodoros erraticus and Ornithodoros moubata

“…Bacterial assembly within arthropod vectors influence pathogen ecology and transmission ( Aželytė et al, 2022 ). The detection of bacterial taxa in the same physical space (i.e., tick tissues) could be an indication of direct interactions between microbes ( Gomard et al, 2021 ).…”

Impact of the microbiome on mosquito-borne diseases

“…One promising approach is to vaccinate vertebrate hosts against mosquito gut bacteria, generating antibodies that target specific bacteria and suppress their growth in mosquitoes, thereby inhibiting pathogen infection. For instance, experimental infection of domestic canaries with Plasmodium relictum , followed by immunization with Enterobacteriaceae, results in the production of bacteria-specific antibodies ( Aželytė et al, 2022 ). Culex quinquefasciatus fed on the infected and immunized birds or birds only immunized have an altered abundance of multiple bacterial taxa in the mosquitoes’ midguts compared to mosquitoes fed on unimmunized counterparts.…”