Increased environmental microbial diversity reduces the disease risk of a mosquitocidal pathogen

Abstract

ABSTRACT Increased diversity in host-associated microbial communities often benefits animal health by provisioning nutrients and protecting against pathogens. In contrast, whether the diversity of environmental microbial communities can also benefit animal health is much less studied. In aquatic environments, water enables environmental microbes to more directly interact with pathogens and animals than in terrestrial environments, which also suggests the potential for community diversity to benefit animal health. In this study, we addressed this question by identifying a strain of Chromobacterium haemolyticum named Rain 0013 ( Ch_ R13) that is a virulent pathogen of mosquito larvae, which live in aquatic habitats. Comparative genomic and functional data suggested many Chromobacterium are both mosquitocidal and opportunistic pathogens of other animals due to conservation of virulence factors that include a broad-spectrum toxin (cyanide). However, we also identified a strongly negative correlation between diversity of the environmental microbiota and disease severity due to Ch_ R13 needing to achieve a threshold density to kill mosquito larvae. Experiments using defined (gnotobiotic) microbial communities further suggested certain environmental community members reduced Ch_ R13 densities more than others. Altogether, our results indicate Ch_ R13 and other Chromobacterium have the potential to broadly cause disease but the environmental communities of microbes in aquatic habitats attenuate disease risk. IMPORTANCE The host-specific microbiotas of animals can both reduce and increase disease risks from pathogens. In contrast, how environmental microbial communities affect pathogens is largely unexplored. Aquatic habitats are of interest because water enables environmental microbes to readily interact with animal pathogens. Here, we focused on mosquitoes, which are important disease vectors as terrestrial adults but are strictly aquatic as larvae. We identified a pathogen of mosquito larvae from the field as a strain of Chromobacterium haemolyticum . Comparative genomic analyses and functional assays indicate this strain and other Chromobacterium are mosquitocidal but are also opportunistic pathogens of other animals. We also identify a critical role for diversity of the environmental microbiota in disease risk. Our study characterizes both the virulence mechanisms of a pathogen and the role of the environmental microbiota in disease risk to an aquatic animal of significant importance to human health.