Carnivorous oyster mushrooms can kill roundworms with “nerve gas in a lollipop”

oyster mushrooms (Pleurotus ostreatus) is a staple of many types of cuisine, with mild flavors and a faint hint of anise. These cream fungi are also one of several types of carnivorous fungi that prey specifically on nematodes (roundworms). The fungus has developed a new mechanism to paralyze and kill its nematode prey: a toxin inside lollipop-like structures called toxocysts that, when released, spread death in minute rounds within tiny cells. Scientists have now identified specific volatile organic compounds for this purpose, according to a new paper published in the journal Science Results.

Carnivorous fungi like oyster mushrooms feed on nematodes because these critters are abundant in the soil and provide a handy source of protein. Other types of various devices were developed for hunting and consuming prey. For example, oomycetes are fungus-like organisms that emit “hunter cells” to search for nematodes. When they find them, they form an anus round the mouth or anus, and then they inject themselves into the worms, which attack the entrails; Another group of oomycetes uses cells that act like predatory harpoons, launching fungal spores into the worm to seal its fate.

Other fungi produce spores with irritating forms such as sticks or stilettos. The spores are swallowed by the nematodes, which are caught in the gullet and germinate by puncturing the worm’s entrails. They are sticky structures like branches that have been swallowed; separating themselves with their bites, when the nematodes swim through them, they inject themselves into the worms; and a dozen or so fungal traps, which are squeezed under the other, killing nematodes.

The oyster mushroom avoids these physical traps in favor of a chemical mechanism. P. ostreatus what is known as “rotten wood” is that they ask for dead trees, but the wood is sometimes poor. The long branched filaments (called hyphae) are part of the bush that grows on rotting wood. Those hyphae are home to toxocysts. When nematodes encounter toxocysts, they rupture, and the nematodes typically become paralyzed and die within minutes. After the prey has died, the hyphae grow into the nematodes’ bodies, dissolving the contents and absorbing nutrients from the dirt.

In 2020, a team of scientists at the Chinese Academy in Taiwan tested all 15 species of P. ostreatus and found that all 15 drops produced noxious fasting. They also tested 17 species of nematodes and found that none survived exposure to the toxin. Co-author Ching-Han Lee and colleagues suggested that the culprit was calcium stored in the animal’s muscles, which, when it responds to nerve signals sent out, causes the muscles to contract. Muscles relax when nerve signals trigger the filling of calcium stores.

To test the hypothesis, the team conducted experiments where calcium was visible in the worms and then investigated the response of the exposed to the oyster toxocyst fungus. They found the pharynx and head of the poisonous muscle nematodes infused with calcium and said the calcium did not go away, leading to widespread nerve and muscle cell death. They suggested that the toxin triggers an initial calcium response, but then jams the mechanism by which the nematodes replenish their calcium supply.

But Lee et al. they were unable to identify the specific toxins responsible for the effects, although they noted that the chemical mechanism of the oyster mushroom is distinct from the nematicides currently used to control nematode populations. For the new study, Lee and co-authors used gas chromatography-mass spectrometry to do just that. The first version of the experiment was tested just containing a vial of sample culture medium and glass beads. A second version was tested containing the sample vial P. ostreatus which had been cultivated for two to three weeks. The third letter was a combination of the first two, testing a vial of sample that contained both cultures P. ostreatus and glass beads.

The culprit: a volatile ketone called 3-octanone, one of several naturally occurring volatile organic compounds (VOCs) that fungi use to communicate. It also appears that 3-octane has a potent nematode-killing mechanism. Exposing four nematode species to 3-octane, the telltale massive (and fatal) influx of calcium ions into nerve and muscle cells. Critical dose, according to the authors. Low doses of slugs and snails are repulsive, but high dosages are deadly. The same is true of nematodes. A high concentration of more than 50 percent 3-octane is required to cause rapid paralysis and widespread cell death. The team also introduced thousands of random genetic changes into the fungus. Those mutants that do not develop toxocysts in their septa are no longer toxic to the nematode Caenorhabditis elegans.

As for why oyster mushrooms have evolved such an unusual mechanism to kill nematodes, the authors suggest that dead or rotting trees are particularly poor in nitrogen, and this mechanism is a good way for the fungi to compensate for that deficiency. Toxocysts could also serve a defensive purpose. Specific nematode species can pierce fungal hyphae to suck out the cytoplasm, so toxocysts that release poisonous gas into the hyphae could protect the fungus from such predators.

DOI: Advanced Science, 2023. 10.1126/sciadv.ade4809 (De DOIs).