On the phenology of protists: Recurrent patterns reveal seasonal variation of protistan (Rhizaria: Cercozoa, Endomyxa) communities in tree canopies

Abstract

Tree canopies are colonized by billions of highly specialized microorganisms that are well adapted to the extreme microclimatic conditions, caused by diurnal fluctuations and seasonal changes. In this study we investigated seasonality patterns of protists in tree canopies of a temperate floodplain forest via high-throughput sequencing with group-specific primers for the phyla Cercozoa and Endomyxa. We observed consistent seasonality and identified divergent spring and autumn taxa. Tree crowns were characterized by a dominance of bacterivores and omnivores, while eukaryvores gained a distinctly larger share in litter and soil communities on the ground. Seasonality was largest among communities detected on the foliar surface. Higher variance within alpha diversity of foliar communities in spring indicated greater heterogeneity during community assembly. However, communities underwent distinct changes during the aging of leaves in autumn, reflecting recurring phenological changes during microbial colonization of leaves. Surprisingly, endomyxan root pathogens appeared to be exceptionally abundant across tree canopies during autumn season, demonstrating a potential role of the canopy surface as an important reservoir for wind-dispersed propagules. Overall, about 80% of detected OTUs could not be assigned to known species - representing only a fraction of dozens of microeukaryotic taxa whose canopy inhabitants are waiting to be discovered.

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

“…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).…”

“…A common pattern in microbial community ecology studies is a high seasonal variability (Nolte et al, 2010;Fiore-Donno et al, 2019;Fournier et al, 2020;Walden et al, 2021).…”

“…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. Accordingly, seasonal variability has been shown to influence protistan communities, to some extent, in several studies (Nolte et al, 2010;Fiore-Donno et al, 2019;Fournier et al, 2020;Walden et al, 2021). For cercozoan communities, Walden et al (2021) could show annually reoccurring succession patterns in the phyllosphere.…”

“…Accordingly, seasonal variability has been shown to influence protistan communities, to some extent, in several studies (Nolte et al, 2010;Fiore-Donno et al, 2019;Fournier et al, 2020;Walden et al, 2021). For cercozoan communities, Walden et al (2021) could show annually reoccurring succession patterns in the phyllosphere. This implied not only spatially, but also seasonally structured cercozoan communities in tree canopies, although this was not reflected on a functional scale.…”

A Parasite’s Paradise: Biotrophic Species Prevail Oomycete Community Composition in Tree Canopies

“…However, the former study only analysed one time point, while the latter study that included air samples could show a strong temporal variability in community composition. Accordingly, several studies have shown that seasonal variability can influence protistan communities, to some extent (Nolte et al, 2010;Fiore-Donno et al, 2019;Fournier et al, 2020;Walden et al, 2021). For cercozoan communities, Walden et al (2021) could show annually reoccurring succession patterns in the phyllosphere.…”