Carnivorous oyster mushrooms can kill roundworms with ‘nerve gas in a lollipop’

oyster mushroom (pleurisy ostreatus) are a staple in many types of cuisines, prized for their mild flavors and mysterious aroma that hints at anise. This cream-colored mushroom is also one of several species of carnivorous fungi that feed on Nematodes (roundworms) in particular. Mushrooms have evolved a new mechanism to paralyze and kill their nematode prey: a toxin found inside lollipop-like structures called toxosomes that, when emitted, causes widespread cell death in nematodes within minutes. Scientists have now identified the specific volatile organic compound responsible for this effect, according to the new leaf Published in the journal Science Advances.

Carnivorous fungi such as oyster mushrooms feed on nematodes because these small creatures are abundant in the soil and provide a useful source of protein. Different species have evolved different mechanisms for hunting and consuming their prey. for example, Omcyts They are fungus-like organisms that send out “hunter cells” to hunt for nematodes. Once found, they form cysts near the roundworm’s mouth or anus and then inject themselves into the worms to attack the internal organs. Another group of albicans uses cells that act like harpoons hunting for prey, injecting fungal spores into the worm to seal its fate.

Other fungi produce spores with irritating stick-like or dagger-like shapes. Nematodes ingest spores that become lodged in the esophagus and germinate by perforating the worm’s intestine. There are sticky, branch-like structures that act like superglue; death collars that detach when nematodes swim through and inject themselves into the worms; More than a dozen fungal species use decoys that collapse in less than a second, squeezing the nematodes to death.

Zoom in / Scanning electron microscopy (SEM) image of toxic cysts P. ostreatus fungal filament.

Yi Yun Lee

Oyster mushrooms avoid these physical traps in favor of a chemical mechanism. P. ostreatus It is what is known as a “wood spinner” that targets dead trees, but the wood is relatively poor in protein. Its long, branching filaments (called filaments) are part of the ‘shroom’ that grows in the rotting wood. This hyphae is the home of the poison cysts. When nematodes encounter the venom cysts, they burst, and the nematodes are usually paralyzed and die within minutes. Once the prey is dead, the hyphae grow into the nematodes’ bodies, dissolving the contents and sucking out the slurry for nutrients.

In 2020, a team of scientists at Academia Sinica in Taiwan tested all 15 species P. ostreatus And I found it All 15 can produce toxic drops when hungry. They also tested 17 species of nematodes and found that none of them could survive exposure to the toxin. Co-author Cheng Han Li and colleagues suggested that the culprit might be calcium stored in the animals’ muscles, which, when released in response to nerve signals, causes the muscles to contract. Muscles relax when nerve signals refill calcium stores.

To test the hypothesis, the team conducted experiments where calcium in the worms was visible, then tracked the response to exposure to oyster mushroom cysts. They found that the pharyngeal and head muscles of the poisoned nematode were flooded with calcium and said that the calcium did not disappear, resulting in widespread neuromuscular cell death. They suggested that the venom triggers the initial response to calcium, but then blocks the mechanism by which the nematodes replenish their calcium supply.

but me et al. They were unable to identify the specific toxins responsible for the effect, although they did note that the chemical mechanism of the oyster mushroom was different from the nematicides currently used to control nematode populations. For the new study, Li and co-authors used a gas chromatography-mass spectrometer to do just that. The first version of the experiment tested a sample vial containing only culture medium and glass beads. A second copy tested a sample containing a vial P. ostreatus that have been reared for two to three weeks. The third copy was a mixture of the first two, test sample vials containing both cultures P. ostreatus and glass beads.

The culprit: a volatile ketone called 3-octanone, which is one of several naturally occurring volatile organic compounds (VOCs) that fungi use to communicate. 3-octanone also appears to act as an effective nematode-killing mechanism. Exposing four species of nematodes to 3-octanone caused a massive (and fatal) influx of calcium ions into nerve and muscle cells. Dosage is critical, according to the authors. Low doses repel slugs and snails, but high doses are fatal. The same applies to nematodes. A high concentration of more than 50 percent of 3-octanone is required to cause rapid paralysis and widespread cell death. The team also caused thousands of random genetic mutations in the fungus. Those mutants that did not develop toxic cysts on their filaments were no longer toxic to nematodes Certain types are elegant.

As for why mushrooms develop such an unusual nematode-killing mechanism, the authors suggest that it is because dying or rotting trees are particularly poor in nitrogen, and this mechanism is a good way for mushrooms to make up for this deficiency. These cysts may even serve a defensive purpose. Certain types of nematodes can pierce fungal hyphae to suck out the cytoplasm, so the presence of toxic gas-emitting cysts on the hyphae could protect the fungi from such predators.

DOI: Science Advances, 2023. 10.1126/sciadv.ade4809 (About DOIs).