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

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ORIGINAL PAPER

Different community compositions between obligate and facultative oomycete plant parasites in a landscape-scale metabarcoding survey Anna Maria Fiore-Donno 1,2

&

Michael Bonkowski 1,2

Received: 7 April 2020 / Revised: 20 October 2020 / Accepted: 23 October 2020 # The Author(s) 2020

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. Keywords Oomycota . Soil food web . Soil protists . Environmental filtering . Plant pathogens . Functional traits

Introduction Oomycetes are protists (phylum Stramenopiles or Heterokonta) ubiquitous and widespread in terrestrial (Geisen et al. 2015; Lara and Belbahri 2011; Singer et al. 2016), freshwater (Duffy et al. 2015) and marine ecosystems (Garvetto et al. 2018). In terrestrial ecosystems, oomycetes occur as pathogens of plants and other eukaryotes and, less commonly, as saprotrophs (Marano et al.

* Anna Maria Fiore-Donno [email protected] Michael Bonkowski [email protected] 1

Terrestrial Ecology Group, Institute of Zoology, University of Cologne, Cologne, Germany

2

Cluster of Excellence on Plant Sciences (CEPLAS), Cologne, Germany

2016), with plant pathogens representing more than 60% of the oomycete taxa (Thines and Kamoun 2010). Wellknown examples are the soil-borne downy mildews with genera like Phytophthora and Pythium and the white rusts (Albugo) on plant leaves (Savory et al. 2015). The genus Pythium is one of the most important soil-borne plant pathogens, being ubiquitous and with an extremely wide host range, attacking the roots of thousands of different plant species (Beakes and Thines 2016). Phytophthora, the “plant destroyer”, is responsible for the widespread rapid tree decline (Hayden et al. 2013) and for damages to important crops like soybean, tomato, grapevine and tobacco (Lebeda et al. 2008). Because of their negativ