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

Abstract

Tree canopies are colonized by billions of highly specialized microorganisms that are well adapted to the highly variable microclimatic conditions, caused by diurnal fluctuations and seasonal changes. In this study we investigated seasonality patterns of protists in the 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. In the canopy seasonality was largest among communities detected on the foliar surface: In spring, higher variance within alpha diversity of foliar samples indicated greater heterogeneity during initial colonization. However, communities underwent compositional changes during the aging of leaves in autumn, highly reflecting recurring phenological changes during protistan colonization. Surprisingly, endomyxan root pathogens appeared to be exceptionally abundant across tree canopies during autumn, demonstrating a potential role of the canopy surface as a physical filter for air-dispersed propagules. Overall, about 80% of detected OTUs could not be assigned to known species—representing dozens of microeukaryotic taxa whose canopy inhabitants are waiting to be discovered.

Pathogen invasion increases the abundance of predatory protists and their prey associations in the plant microbiome

“…The responses of these communities to pathogen invasion have been extensively studied in various agricultural crops (Berendsen et al, 2018;Carrión et al, 2019;Gao et al, 2021;Kwak et al, 2018;Liu et al, 2020). Our component that is highly sensitive to fertilization (Guo et al, 2021;Zhao et al, 2019), aridity (Chen et al, 2022) and seasonal variation (Walden et al, 2021). Expanding upon these observations, our findings indicate that disease resulting from pathogen invasion can markedly alter soil-and plant-associated protistan communities.…”

“…Protists are important components of soil and plant microbiomes, and their communities are influenced by factors such as plant compartments, sampling sites and plant health. Previous studies have shown that protists constitute a significant microbial component that is highly sensitive to fertilization (Guo et al., 2021; Zhao et al., 2019), aridity (Chen et al., 2022) and seasonal variation (Walden et al., 2021). Expanding upon these observations, our findings indicate that disease resulting from pathogen invasion can markedly alter soil‐ and plant‐associated protistan communities.…”

Illuminating protist diversity in pitcher plants and bromeliad tanks

“…Previous research has shown a similar pattern for bacteria and protists where seasonal dynamics can lead to community homogenization over time [ 51 – 54 ]. Bacteria in the phyllosphere have clear seasonal patterns dependent on priority effects whereby the success of one early strain influences the outcome of the entire community [ 51 , 55 ].…”

Inter‐ and intraspecific phytochemical variation correlate with epiphytic flower and leaf bacterial communities

“…Although little is known about microbial transmission and succession on plant surfaces, any transmission event may cause a change in microbial flora, depending on the type and quantity of new arrivals. Dispersal by pollinators has been shown for bacteria and fungi (Keller et al, 2021; Rebolleda Gómez & Ashman, 2019; Vannette, 2020), and even suggested for low amount protists that may act as bacterial predators (Walden et al, 2021). Furthermore, the diversity of arthropods potentially interacting with plants has been shown to affect bacterial composition and diversity on flowers and leaves (Junker, Eisenhauer, et al, 2021).…”