Nematode-Trapping Fungi Produce Diverse Metabolites during Predator-Prey Interaction.

Ting-Hao Kuo,Ching-Ting Yang,Yen-Ping Hsueh,Hsin-Yuan Chang,Cheng-Chih Hsu

doi:10.3390/metabo10030117

Ting-Hao Kuo, Ching-Ting Yang + Show 3 more

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https://doi.org/10.3390/metabo10030117

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Journal: Metabolites	Publication Date: Mar 20, 2020
Citations: 25	License type: CC BY 4.0

Affiliation: National Taiwan University

Abstract

Nematode-trapping fungi are natural antagonists of nematodes. These predatory fungi are capable of switching their lifestyle from a saprophytic to predatory stage in the presence of nematodes by developing specialized trapping devices to capture and consume nematodes. The biochemical mechanisms of such predator–prey interaction have become increasingly studied given the potential application of nematode-trapping fungi as biocontrol agents, but the involved fungal metabolites remain underexplored. Here, we report a comprehensive liquid–chromatography mass spectrometry (LC–MS) metabolomics study on one hundred wild isolates of nematode-trapping fungi in three different species, Arthrobotrys oligospora, Arthrobotrys thaumasia, and Arthrobotrys musiformis. Molecular networking analysis revealed that the fungi were capable of producing thousands of metabolites, and such chemical diversity of metabolites was notably increased as the fungi switched lifestyle to the predatory stage. Structural annotations by tandem mass spectrometry revealed that those fungal metabolites belonged to various structural families, such as peptide, siderophore, fatty alcohol, and fatty acid amide, and their production exhibited species specificity. Several small peptides (<1.5 kDa) produced by A. musiformis in the predatory stage were found, with their partial amino acid sequences resolved by the tandem mass spectra. Four fungal metabolites (desferriferrichrome, linoleyl alcohol, nonadecanamide, and citicoline) that were significantly enriched in the predatory stage were identified and validated by chemical standards, and their bioactivities against nematode prey were assessed. The availability of the metabolomics datasets will facilitate comparative studies on the metabolites of nematode-trapping fungi in the future.

Highlights

Nematode-trapping fungi (NTF) are an intriguing class of carnivorous microorganisms that are capable of developing specialized predatory devices to trap and digest nematodes [1]
The detected fungal metabolites were visualized as molecular networks basing on their tandem mass spectral similarities (Figure 2a for the organic extract; Figure S1 for the aqueous extract)
We showed that the Arthrobotrys metabolomic dataset yielded 12,179 nodes and hundreds of molecular clusters spanning in the molecular network (Figure 2a and Figure S1)

Summary

Introduction

Nematode-trapping fungi (NTF) are an intriguing class of carnivorous microorganisms that are capable of developing specialized predatory devices to trap and digest nematodes [1]. More than 200 species of NTF have been described to date, and they are broadly distributed in terrestrial and aquatic ecosystems [2]. NTF are natural antagonists of nematodes, which are crucial crop pests and cause agricultural damage worldwide. The global financial loss due to plant-parasitic nematodes is estimated to be over USD 100 billion [3,4]. To address this problem, NTF, serve as ecophysiological sources of novel biological control agents that are beneficial to agriculture and ecosystems

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