Sensory cilia as the Achilles heel of nematodes when attacked by carnivorous mushrooms

Abstract

Fungal predatory behavior on nematodes has evolved independently in all major fungal lineages. The basidiomycete oyster mushroomPleurotus ostreatusis a carnivorous fungus that preys on nematodes to supplement its nitrogen intake under nutrient-limiting conditions. Its hyphae can paralyze nematodes within a few minutes of contact, but the mechanism had remained unclear. We demonstrate that the predator–prey relationship is highly conserved between multiplePleurotusspecies and a diversity of nematodes. To further investigate the cellular and molecular mechanisms underlying rapid nematode paralysis, we conducted genetic screens inCaenorhabditis elegansand isolated mutants that became resistant toP. ostreatus. We found that paralysis-resistant mutants all harbored loss-of-function mutations in genes required for ciliogenesis, demonstrating that the fungus induced paralysis via the cilia of nematode sensory neurons. Furthermore, we observed thatP. ostreatuscaused excess calcium influx and hypercontraction of the head and pharyngeal muscle cells, ultimately resulting in rapid necrosis of the entire nervous system and muscle cells throughout the entire organism. This cilia-dependent predatory mechanism is evolutionarily conserved inPristionchus pacificus, a nematode species estimated to have diverged fromC. elegans280 to 430 million y ago. Thus,P. ostreatusexploits a nematode-killing mechanism that is distinct from widely used anthelmintic drugs such as ivermectin, levamisole, and aldicarb, representing a potential route for targeting parasitic nematodes in plants, animals, and humans.

Genomic analyses of two Italian oyster mushroomPleurotus pulmonariusstrains

“…We further discovered that ss2 and ss5 exhibited differences in toxicity towards the nematode Caenorhabditis elegans. All nematodes in contact with the mycelium of ss5 were paralyzed after 10 minutes exposed to the fungal hyphae, which was comparable to previous studies of Pleurotus species (Thorn and Barron 1984;Lee et al 2020). In contrast, the mycelium of ss2 showed a much weaker toxicity toward C. elegans, being able to paralyze only ~40% of the nematode population tested ( Figure 1B).…”

“…One of the most unknown characteristics of Pleurotus mushrooms is their ability to kill and feed on living nematodes (Thorn and Barron 1984) and therefore their potential for the biocontrol of parasitic nematodes (Degenkolb and Vilcinskas 2016; Sivanandhan et al 2017;Castañeda-Ramírez et al 2020). Although a few compounds produced by Pleurotus have been reported to cause paralysis in nematode worms (Kwok et al 1992;Satou et al 2008), a more recent study has suggested that the true identity of the toxins targeting nematodes remain to be discovered (Lee et al 2020).…”

Mechanism of murderous mushrooms paves path for parasitic helminth halt

“…Single-nucleotide polymorphism mapping and whole-genome sequencing revealed nine independent, loss-of-function mutations in genes, all of which are essential for the development of ciliated sensory neurons or amphid channel morphogenesis, the latter representing the nose of the worm, the most crucial sensory organ of these blind creatures. Using these mutants along with previously established lines with known defects in either the function of ciliated sensory neurons or impaired signaling, Lee et al (7) surprisingly found that the intact cilia structure, but not sensory neural function, is needed to elicit paralysis. However, mutants with defects in ciliated sensory neuron development displayed a range of paralysis upon hyphae contact, suggesting that several factors are at play.…”

“…Other fungi use infective spores that either bind to the nematode cuticle or are ingested (6). As explored in PNAS by Lee et al (7), the eatable oyster mushroom Pleurotus ostreatus of the Basidiomycota uses yet another mechanism by employing toxin-induced paralysis to kill its prey. While the predatory capacities of fungi are well established, the execution mechanisms are gradually being elucidated.…”

Genome sequence of the oyster mushroomPleurotus ostreatusstrain PC9

“…Another potential toxin, linoleic acid, reduces nematodes head size (Satou et al 2008). When nematodes contact the mycelium of P. ostreatus, fungal toxins enter the prey through their sensory cilia, leading to hypercontraction and calcium influx of pharyngeal and body wall muscles, ultimately causing necrosis process of the neuromuscular system (Lee et al 2020). However, the identity of the toxins and how exactly P. ostreatus induces rapid cell necrosis remain unclear.…”