Different community compositions between obligate and facultative oomycete plant parasites in a landscape-scale metabarcoding survey

Abstract

Oomycetes are a ubiquitous protistan lineage including devastating crop parasites. Although their ecology in agrosystems has been widely studied, little is known of their distribution in natural and semi-natural ecosystems and how they respond to edaphic and environmental factors. We provide here a baseline of the diversity and distribution of soil oomycetes, classified by lifestyles (biotrophy, hemibiotrophy and saprotrophy), at the landscape scale in temperate grassland and forest. From 600 soil samples, we obtained 1148 operational taxonomy units representing ~ 20 million Illumina reads (region V4, 18S rRNA gene). We found a majority of hemibiotrophic plant pathogens, which are parasites spending part of their life cycle as saprotrophs after the death of the host. Overall both grassland and forest constitute an important reservoir of plant pathogens. Distance-based RDA models identified soil type and mineral soil C/N ratio as the most influential factors in shaping oomycete communities in grassland and forest. Edaphic conditions and human-induced management intensification in forest triggered opposite responses in the relative abundances of obligate biotrophs and hemibiotrophs, suggesting different ecological requirements of these two lifestyles.

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

“…Recent molecular studies analysing oomycete diversity determined patterns similar to those reflected in our study, i.e., soil habitats are dominated by hemibiotrophic species, mostly members of the Pythiales (Sapkota and Nicolaisen, 2015;Riit et al, 2016;Fiore-Donno and Bonkowski, 2021). Species of the genus Pythium were significantly differentially abundant in the sampled ground habitats.…”

“…The significant differential abundance in the canopy of several undetermined OTUs that can only be assigned to the family Pythiaceae (Figure 4) indicates hitherto undescribed lineages, specialised on the survival in the canopy. Members of the Pythiaceae can occupy all lifestyles, from saprotrophy over hemibiotrophy to obligate biotrophy (Fawke et al, 2015;Marano et al, 2016;Fiore-Donno and Bonkowski, 2021). If the OTUs in the canopy would show an obligate biotrophic lifestyle, it would be in line with observations of the other lineages in the canopy (Figure 1).…”

“…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 and Fry, 2006). The ecological and economic impact of oomycetes has led to an increased research interest on their community structure (Riit et al, 2016;Singer et al, 2016;Jauss et al, 2020a,b;Fiore-Donno and Bonkowski, 2021;Marčiulynienė et al, 2021), and, correspondingly, their pathogenicity and infection strategies (Rizzo and Garbelotto, 2003;Rizzo et al, 2005;Thines and Kamoun, 2010).…”

“…Oomycete communities are well studied in terrestrial habitats, however, most studies focus on soil and the rhizosphere (Arcate et al, 2006;Esmaeili Taheri et al, 2017;Sapp et al, 2019;Fiore-Donno and Bonkowski, 2021). Recently, Jauss et al (2020b) characterised oomycete diversity and community composition in tree canopies, which are huge ecosystems containing heterogeneous microhabitats and a large proportion of undescribed diversity (Nadkarni, 2001).…”

From Forest Soil to the Canopy: Increased Habitat Diversity Does Not Increase Species Richness of Cercozoa and Oomycota in Tree Canopies

“…The thermal program for the first and second PCR consisted of an initial denaturation step at 95°C for 2 min, 24 cycles at 95°C for 30 s, 52°C for 30 s, 72°C for 30 s; and a final elongation step at 72°C for 5 min. For amplifying the ITS 1 of the oomycete communities, we used the specific primer pair ITS_177F and 58SR_Oom ( Fiore-Donno and Bonkowski, 2020 ). Amplicons of the first PCR were again used as template for a semi-nested PCR with the primer pair I1786F_Stra and 58SR_Oom.…”