Host-mediated niche construction of bacterial communities in an aquatic microecosystem

Microbes coordinate homeostasis in host-associated and environmental ecosystems alike, but the connectivity of these biomes is seldom considered. Hosts exert controls on the composition and function of their internally associated symbionts, but an underappreciated modality of microbiome curation is external to the host through changes to the environmental species pool from which they recruit microbial symbionts. Niche construction theory describes how organisms alter their environment and the selective landscape of their offspring and conspecifics. We hypothesize that host-driven manipulation of environmental microbial communities is an underexplored form of this concept. Using the pitcher plant mosquito (Wyeomyia smithii) as a model, we tested how hosts shape microbial communities across developmental stages and gradients of pre-existing community complexity. We report three lines of evidence supporting host-mediated niche construction, leveraging amplicon sequencing and microbiota manipulation experiments with germ-free (axenic) and selectively recolonized (gnotobiotic) mosquitoes. First, single female egg-laying assays showed repeatable adult inoculation of sterile water with beneficial bacteria capable of sustaining robust larval development. Second, increasing larval density in assays inoculated with complex, field-derived microbial communities selected for environmental and host-associated bacteria that correlated with increased larval fitness. Finally, exposing axenic larvae to mixtures of parentally and environmentally derived microbiota demonstrated that prior conditioning by conspecifics enhanced offspring fitness. Although the bacterial taxa associated with mosquito structuring varied, members of the Actinobacteriota and Acetobacteraceae were consistently associated with increased fitness. Overall, our results provide an example of host-mediated niche construction to favor environmental microbial communities that positively impact host fitness.