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

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Edited by Paul W. Sternberg, California Institute of Technology, Pasadena, CA, and approved January 27, 2020 (received for review October 22, 2019)This article requires a subscription to view the full text. If you have a subscription you may use the login form below to view the article. Access to this article can also be purchased.Multiple fungal lineages have independently evolved carnivorous behaviors, preying on a diversity of nematodes as an adaptation for survival in low-nutrient environments. The edible oyster mushroom Pleurotus ostreatus is known to paralyze nematode prey, but the mechanism was unclear. We show that P. ostreatus triggers a massive calcium influx and rapid cell necrosis in the neuromuscular system of C. elegans via that nematode’s sensory cilia—a mode of action that is conserved across nematodes. Our study reveals a rapid killing mechanism that has not been described previously and is distinct from that employed by common anthelmintic drugs, representing a potential route for targeting parasitic nematodes. It also establishes a paradigm for studying cell death in C. elegans.Fungal predatory behavior on nematodes has evolved independently in all major fungal lineages. The basidiomycete oyster mushroom Pleurotus ostreatus is 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 multiple Pleurotus species and a diversity of nematodes. To further investigate the cellular and molecular mechanisms underlying rapid nematode paralysis, we conducted genetic screens in Caenorhabditis elegans and isolated mutants that became resistant to P. 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 that P. ostreatus caused 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 in Pristionchus pacificus, a nematode species estimated to have diverged from C. elegans 280 to 430 million y ago. Thus, P. ostreatus exploits 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.Published under the .You may purchase access to this article. This will require you to if you don't already have one.Subscribers, for more details, please visit our .Please click to log into the PNAS submission website.Sensory cilia as the Achilles heel of nematodes when attacked by carnivorous mushroomsSensory cilia as the Achilles heel of nematodes when attacked by carnivorous mushroomsWhile some sustainable development efforts will reduce emerging disease risk, others may increase it—suggesting important lessons for the coronavirus outbreak and beyond.Image credit: Pixabay/sasint.QnAs with NAS member and bioengineer Sangeeta Bhatia.Image courtesy of Howard Hughes Medical Institute/Scott Eisen.An ancient bead-making settlement on a Florida coastal island was crucial to pre-Columbian economies.Image courtesy of Terry E. Barbour and Kenneth E. Sassaman.A beetle preserved in Burmese amber suggests early evidence of insect pollination of flowering plants.Image courtesy of Bo Wang.A study explores the pervasiveness of plastics in fish nurseries and suggests plastic accumulation in larval fish nurseries may affect marine ecosystems.Image courtesy of Jonathan L. Whitney.

Edited by Paul W. Sternberg, California Institute of Technology, Pasadena, CA, and approved January 27, 2020 (received for review October 22, 2019)This article requires a subscription to view the full text. If you have a subscription you may use the login form below to view the article. Access to this article can also be purchased.Multiple fungal lineages have independently evolved carnivorous behaviors, preying on a diversity of nematodes as an adaptation for survival in low-nutrient environments. The edible oyster mushroom Pleurotus ostreatus is known to paralyze nematode prey, but the...

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