Oyster Mushrooms (Pleurotus ostreatus) is a staple of many types of cuisine, prized for its mild flavors and vaguely aniseed scent. These cream-colored mushrooms are also one of many types of carnivorous fungi that particularly attack nematodes (roundworms). Fungi have evolved a new mechanism to paralyze and kill their nematode prey: a toxin contained in lollipop-like structures called toxocysts which, when released, cause widespread cell death in roundworms within minutes. Scientists have now identified the specific volatile organic compound responsible for this effect, according to a new paper published in the journal Science Advances.
Carnivorous fungi like the oyster mushroom feed on nematodes because these little creatures are abundant in the soil and provide a convenient source of protein. Different species have evolved various mechanisms to hunt and consume their prey. For example, oomycetes are fungus-like organisms that send out “hunter cells” in search of nematodes. Once found, they form cysts near the roundworms mouth or anus, then inject themselves into the worms to attack the internal organs. Another group of oomycetes use cells that behave like harpoons in search of prey, injecting the fungal spores into the worm to seal its fate.
Other fungi produce spores in irritating shapes like rods or stilettos. The nematodes swallow the spores, which get stuck in the esophagus and germinate, perforating the intestine of the worm. There are sticky branch-like structures that act like superglue; death collars that come off when nematodes swim through them, injecting themselves into the worms; and a dozen fungal species use traps that tighten in less than a second, squeezing nematodes to death.
To test the hypothesis, the team conducted experiments where calcium in the worms was visible, then followed the response to exposure to oyster mushroom toxocysts. They found that the pharynx and head muscles of poison nematodes were flooded with calcium and the calcium did not disappear, leading to widespread nerve and muscle cell death. They suggested that the toxin triggers the initial calcium response, but then blocks the mechanism by which nematodes replenish their calcium supply.
But Lee et al. might not identify the specific toxins responsible for the effect, although they noted that the chemical mechanism of the oyster mushroom was distinct from the nematicides currently used to control nematode populations. For the new study, Lee and his co-authors used gas chromatography and mass spectrometry to achieve this. The first version of the experiment tested a sample flask containing only the culture medium and glass beads. A second version tested a sample vial containing P. ostreatus which had been grown for two to three weeks. The third version was a combination of the first two, testing a vial sample containing both cultures P. ostreatus and glass beads.
The culprit: a volatile ketone called 3-octanone, one of many naturally occurring volatile organic compounds (VOCs) that fungi use to communicate. It appears that 3-octanone also serves as a potent nematode killing mechanism. Exposure of four species of nematodes to 3-octanone triggered the telltale massive (and lethal) influx of calcium ions into nerve and muscle cells. Dosage is critical, according to the authors. Low doses are a slug and snail repellent, but high doses are deadly. The same is true for nematodes. A high concentration of over 50% 3-octanone is required to trigger rapid paralysis and widespread cell death. The team also induced thousands of random genetic mutations in the fungus. Mutants that did not develop toxocysts on their hyphae were no longer toxic to the nematode Caenorhabditis elegans.
As to why oyster mushrooms have evolved such an unusual mechanism for killing nematodes, the authors suggest it’s because dying or rotting trees are particularly low in nitrogen, and this mechanism is a good way for fungi to compensate for this. deficiency. The toxocysts might even serve a defensive purpose. Specific nematode species can pierce fungal hyphae to suck up the cytoplasm, so having toxocysts that emit poisonous gases on the hyphae might protect the fungus from these predators.
DOI: Science Advances, 2023. 10.1126/sciadv.ade4809 (About DOIs).