Natural diversity in the predatory behavior facilitates the establishment of a robust model strain for nematode-trapping fungi

Abstract

Nematode-trapping fungi (NTF) are a group of specialized microbial predators that consume nematodes when food sources are limited. Predation is initiated when conserved nematode ascaroside pheromones are sensed, followed by the development of complex trapping devices. To gain insights into the coevolution of this interkingdom predator–prey relationship, we investigated natural populations of nematodes and NTF that we found to be ubiquitous in soils.Arthrobotrysspecies were sympatric with various nematode species and behaved as generalist predators. The ability to sense prey among wild isolates ofArthrobotrys oligosporavaried greatly, as determined by the number of traps after exposure toCaenorhabditis elegans. While some strains were highly sensitive toC. elegansand the nematode pheromone ascarosides, others responded only weakly. Furthermore, strains that were highly sensitive to the nematode prey also developed traps faster. The polymorphic nature of trap formation correlated with competency in prey killing, as well as with the phylogeny ofA. oligosporanatural strains, calculated after assembly and annotation of the genomes of 20 isolates. A chromosome-level genome assembly and annotation were established for one of the most sensitive wild isolates, and deletion of the only G-protein β-subunit–encoding gene ofA. oligosporanearly abolished trap formation. In summary, our study establishes a highly responsiveA. oligosporawild isolate as a model strain for the study of fungus–nematode interactions and demonstrates that trap formation is a fitness character in generalist predators of the nematode-trapping fungus family.

Fungi–Nematode Interactions: Diversity, Ecology, and Biocontrol Prospects in Agriculture

“…Studies of nematophagous fungi and their interactions with nematodes have revealed several mechanisms of their interactions at the molecular, cellular, organismal, and ecological levels. Indeed, such studies have propelled their interactions as models for studying inter-kingdom interactions in predator–prey coevolution, and for biocontrol applications [ 23 , 24 , 25 , 26 , 27 , 28 , 29 ].…”

Genetic Variation in Caenorhabditis elegans Responses to Pathogenic Microbiota

“…Further, it may aid to understand how microbiota influence the fitness of C. elegans and how functional genes affect the microbiota interactions. For example, a recent study on nematode trapping fungi (NTF) demonstrated the trap induction, involving G protein β-subunit Gpb 1, plays as fitness character in NTF family [56]. A next step would be to combine different microbiota, like bacteria and viruses, in order to assess their impact simultaneously.…”

Forward genetic screens identified mutants with defects in trap morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora

“…Arthrobotrys oligospora strain TWF154 was used in this study, a wild isolate we have sampled in Taiwan. Genomic data on this strain can be accessed from the National Center for Biotechnology Information GenBank under accession number SOZJ00000000 (Yang et al, 2020). All corresponding knockout mutants were obtained in a ku70 strain background.…”

“…More than 200 of these nematodetrapping fungi (NTF) have been described to date, with Arthrobotrys oligospora being the best studied species (Nordbring-Hertz et al, 2011). A. oligospora is known to eavesdrop on nematode ascaroside pheromones to trigger trap morphogenesis and to produce volatile compounds mimicking food and sex cues that lure nematodes, and predatory abilities among natural populations of this species can vary considerably (Hsueh et al, 2017;Hsueh et al, 2013;Yang et al, 2020).…”

“…These include the mitogen-activated protein kinase (MAPK), Slt2, which is involved in the cell wall integrity signaling pathway in yeast (Zhen et al, 2018), a pH-sensing receptor, palH, that functions in the pH signal transduction pathway, and a NADPH oxidase, NoxA, that controls ROS signaling responses in A. oligospora (Li et al, 2019;Li et al, 2017). More recently, it has been demonstrated that the G protein beta subunit, Gpb1, is required for the predatory lifestyle transition in A. oligospora (Yang et al, 2020).…”