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

Abstract

Oomycetes (Stramenopiles, protists) are among the most severe plant pathogens, comprising species with a high economic and ecologic impact on forest ecosystems. Their diversity and community structures are well studied in terrestrial habitats, but tree canopies as huge and diverse habitats have been widely neglected. A recent study highlighted distinct oomycete communities in the canopy stratum compared to the ground region of three temperate deciduous trees (Quercus robur, Tilia cordata, Fraxinus excelsior). While the communities from the two strata were distinct when taking oomycete abundances into account, they were rather similar when only OTU presence/absence was considered. It remains, however, unknown if this homogeneity in the OTU presence also leads to a functional homogenisation among microhabitats within the two strata ground and canopy. In this study, we supplemented functional traits to oomycete communities in the tree microhabitats, which were determined over a time period of 2 years with a metabarcoding approach. Our results showed that even though most oomycetes occurred in all microhabitats, a strong discrepancy between the strata and correspondingly the distribution of oomycete lifestyles could be observed. This pattern was constant over several seasons. Obligate biotrophic species, exclusively feeding on living host tissue, dominated the canopy region, implying tree canopies to be a hitherto neglected reservoir for parasitic protists. OTUs assigned to the genus Hyaloperonospora—parasites highly specialised on hosts that were not sampled—could be determined in high abundances in the canopy and the surrounding air, challenging the strict host dependencies ruled for some oomycetes. Our findings further contribute to the understanding of oomycete ecosystem functioning in forest ecosystems.

Conceptual analysis: What signals might plant canopies send via stemflow?

“…For host trees, their epiphytes and epifauna, microbiota can engage in various relationships of interest, including mutualism (Mejía et al, 2014), saprotrophism (Song et al, 2017), and pathogenism (Laine et al, 2014), though many, of course, have no known relationship. Parasitic and pathogenic signals in stemflow samples may be useful to assess the extent and severity of microbial disease agents, from viruses (D'Amico and Elkinton, 1995) and bacteria (Griffin and Carson, 2015), to protists, especially a group of particularly effective plant pathogens, oomycetes (Jauss et al, 2021). Viruses can travel in the waters draining through canopies, originating from literal reservoirs of water, like dendrotelmata (Kollars et al, 2019;Diouf et al, 2020), and from cadaverous reservoirs, like putrefying gypsy moths (D'Amico and Elkinton, 1995).…”

“…These studies report that fungal conidia can be abundant in stemflow: up to billions of conidia ha −1 y −1 (Magyar et al, 2021). It has been recently observed that tree canopies can hold more species of parasitic oomycetes with lifestyles that exclusively feed on living host tissue than in other forest compartments, implying tree canopies may themselves be a major reservoir for parasitic protists (Jauss et al, 2021). As stemflow washes much of the canopy, it may provide an integrated signal of this parasitic protist community and its compositional or functional dynamics.…”