Microhabitat Governs the Microbiota of the Pinewood Nematode and Its Vector Beetle: Implication for the Prevalence of Pine Wilt Disease.

Our understanding of environmental acquisition of microbes and migration-related alteration of microbiota across habitats has rapidly increased. However, in complex life cycles, such as for many parasites, exactly how these microbes are transmitted across multiple environments, such as hosts and habitats, is unknown. Pinewood nematode, the causal agent of the globally devastating pine wilt disease, provides an ideal model to study the role of microbiota in multispecies interactions because its successful host invasion depends on the interactions among its vector insects, pine hosts, and associated microbes. Here, we studied the role of bacterial and fungal communities involved in the nematode's life cycle across different micro- (pupal chamber, vector beetle, and dispersal nematodes) and macrohabitats (geographical locations). We identified the potential sources, selection processes, and keystone taxa involved in the host pine-nematode-vector beetle microbiota interactions. Nearly 50% of the microbiota in vector beetle tracheae and ~60% that of third-stage dispersal juveniles were derived from the host pine (pupal chambers), whereas 90% of bacteria of fourth-stage dispersal juveniles originated from vector beetle tracheae. Our results also suggest that vector beetles' tracheae selectively acquire some key taxa from the microbial community of the pupal chambers. These taxa will be then enriched in the dispersal nematodes traveling in the tracheae and hence likely transported to new host trees. Taken together, our findings contribute to the critical information toward a better understanding of the role of microbiota in pine wilt disease, therefore aiding the knowledge for the development of future biological control agents.