Fatal attraction of Caenorhabditis elegans to predatory fungi

Salicylic acid is a phenolic phytohormone which controls plant growth and development. A methyl ester (MSA) derivative thereof is volatile and involved in plant-insect or plant-plant communication. Here we show that the nematode-trapping fungus Duddingtonia flagrans uses a methyl-salicylic acid isomer, 6-MSA as morphogen for spatiotemporal control of trap formation and as chemoattractant to lure Caenorhabditis elegans into fungal colonies. 6-MSA is the product of a polyketide synthase and an intermediate in the biosynthesis of arthrosporols. The polyketide synthase (ArtA), produces 6-MSA in hyphal tips, and is uncoupled from other enzymes required for the conversion of 6-MSA to arthrosporols, which are produced in older hyphae. 6-MSA and arthrosporols both block trap formation.

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Fig:The artA gene cluster is required for 6-MSA and arthrosporol biosynthesis:a Comparison of colonies of wild-type (WT), a ΔartA- (strain SXY05), aΔartB- (strain SXY15), a ΔartC- (strain SXY14), and a ΔartD-deletion strain (strain SXY16) after 8 days of growth on PDA agar plates. b Trap formation in WT and the ∆artA-deletion strain (scale bar, 100 µm). c Quantification of traps induced by the same number of C. elegans N2 in D. flagrans strains as indicated (mean ± SD, n = 5 biological with 3 technical replicates; asterisks represent significance levels as determined with the unpaired t-test compared to WT; *p < 0.05, **p < 0.01, ***p < 0.001; ΔartA p-value = 3.36858E-06, ΔartB p= 0.097611834; ΔartC p= 9.20668E-07, ΔartD p= 0.002468371). dHPLC-DAD profiles of the extracts of the strains indicated. e LC–MS/MS quantification of 6-MSA from culture extracts of the strains indicated. Ao-artA (strain SXD01) means A. oryzae expressing artA. f Inhibition of D. flagrans by extracts of different strains. D. flagrans was point inoculated and 30 µl of the metabolite extracts added. The plate was incubated for 3 days at 28 °C. Source data are provided as a Source Data file.

The presence of nematodes inhibits 6-MSA and arthrosporol biosyntheses and thereby enables trap formation. 6-MSA and arthrosporols are thus morphogens with some functions similar to quorum-sensing molecules. We show that 6-MSA is important in interkingdom communication between fungi and nematodes.

Yu, X., Hu, X., Pop, M. et al. Fatal attraction of Caenorhabditis elegansto predatory fungi through 6-methyl-salicylic acid. Nat Commun 12,5462 (2021). https://doi.org/10.1038/s41467-021-25535-1

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