To the canopy and beyond: Air samples reveal wind dispersal as a driver of ubiquitous protistan pathogen assembly in tree canopies

Abstract

We analyzed air dispersal of the protistan phyla Cercozoa and Oomycota with an air sampler near the ground (~2 m) and in tree crowns (~25 m) of three tree species (oak, linden and ash) in a temperate floodplain forest in March (before leafing) and May (after leaf unfolding) with a cultivation-independent high throughput metabarcoding approach. Both, Cercozoa and Oomycota, contain important pathogens of forest trees and other vegetation. We found a high diversity of Cercozoa and Oomycota in air samples with 122 and 81 OTUs, respectively. Especially oomycetes showed a high temporal variation in beta diversity between both sampling dates. Differences in community composition between air samples in tree canopies and close to the ground were however negligible, and also tree species identity did not affect communities in air samples, indicating that the distribution of protistan propagules through the air was not spatially restricted in the forest ecosystem. OTUs of plant pathogens, whose host species that did not occur in the forest, demonstrate wind dispersal of propagules from outside the forest biome. Overall, our results lead to a better understanding of the stochastic processes of wind dispersal of protists and protistan pathogens, a prerequisite to understand the mechanisms of their community assembly in forest ecosystems. ImportanceWind dispersal has been shown to play a crucial role in protistan community assembly. The protistan taxa Cercozoa and Oomycota contain important plant parasites with a major ecologic and economic impact. However, comprehensive assessments of cercozoan and oomycete diversity in forest air samples were lacking. Using a cultivation-independent high throughput metabarcoding approach, we analyzed cercozoan and oomycete air dispersal in forest floors and the canopy region - a potential filter for microbial propagules. Our study provides insights into the diversity and community assembly of protists within the air, contributing to a better understanding which factors drive the distribution of plant pathogens within forest ecosystems.