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.

A parasite’s paradise: Biotrophic species prevail oomycete community composition in tree canopies

“…Oomycete community compositions were in fact slightly, yet significantly distinct for every sampling and correspondingly for every season (Table 1). This pattern is in line with hypotheses proposed by Jauss et al (2020a), that seasonal variation in air samples drives the community composition in forest ecosystems. The environment, however, then selects the species most adapted to the microhabitat, leading to overall similar community patterns and microhabitat differences for every season ( Figure 5).…”

“…Comparing the data from Spring 2019 ( Figure 1D,H) with air samples previously published by Jauss et al (2020a) (Figure 2) revealed that the air surrounding canopy and ground habitats was dominated by obligate biotrophic OTUs, irrespective of incidence or abundance.…”

“…Habitats in the canopy, however, were dominated by the obligate biotrophic genera Peronospora and Hyaloperonospora (Figure 4). Tree canopies have only recently been subject to studies on microbial diversity (Jauss et al, 2020a(Jauss et al, , 2020bWalden et al, 2021;Herrmann et al, 2021), indicating tree canopies to be a hitherto neglected reservoir for parasitic microorganisms. Species of the genus Hyaloperonospora are known to be highly host-specific, infecting plant species of Brassicaceae and closely related families (Lee et al, 2017 and references therein).…”

“…The infamous oomycete Phytophthora infestans causes one of the most destructive plant diseases, the potato late blight, and initiated the great Irish famine in the late 1840's with a million deaths and massive emigration (Mizubuti & Fry, 2006). The ecological and economic impact of oomycetes has led to an increased research interest on their community structures (Robideau et al, 2011;Riit et al, 2016;Singer et al, 2016;Jauss et al, 2020bJauss et al, , 2020a, and, correspondingly, their pathogenicity and infection strategies (Rizzo & Garbelotto, 2003;Rizzo et al, 2005;Thines & Kamoun, 2010).…”

“…Albeit the same oomycetes were present on the ground and in the canopy, communities inhabiting canopy habitats were significantly distinct from soil and leaf litter communities in their abundances. The authors concluded that oomycete diversity in forest ecosystems is shaped by deterministic microhabitat filtering, while a study by Jauss et al (2020a) could determine air dispersal and convective transport to be the stochastic supplier and distributor of oomycetes among microhabitats and strata. However, the former study only analysed one time point, while the latter study dealing with air samples could show a strong temporal variability in community composition.…”