To survive on low-nitrogen substrates, oyster mushrooms kill and eat tiny nematodes. A new study now provides insights into their hunting strategy. Accordingly, the fungi form a kind of small lollipops on their subterranean threads that are filled with the nerve gas 3-octanone. When touched by a prey animal, the beads burst and release their poison. The research team simulated the effect in the laboratory: the roundworm is quickly paralyzed and its cells perish. The fungus can now grow into its prey and digest it. The results could help to use oyster mushrooms to combat harmful nematodes in agriculture.
Oyster mushrooms (Pleurotus ostreatus) typically grow on decaying deciduous trees. Since nitrogen is extremely scarce in this environment, they have specialized in killing tiny roundworms, so-called nematodes, and consuming them as a source of nitrogen. For some oyster mushrooms, hunting also serves as a means of defence: depending on the habitat, the nematodes also include specimens that feed on fungal hyphae. Although oyster mushrooms were already known to use chemical compounds to paralyze and kill their prey, their exact strategy was previously unclear.
Lollipops with nerve poison
Previous studies had already looked for the chemical compound that oyster mushrooms use against nematodes. However, although some of the substances that researchers isolated from the fungi were actually able to kill roundworms, none of the previously known compounds triggered the rapid paralysis and cell necrosis observed in nature. “This indicated that the main nematode-killing compound produced by oyster mushrooms had yet to be identified,” writes a team led by Ching-Han Lee of the Academia Sinica in Taiwan.
To find the corresponding toxin and uncover the mechanism, the team conducted a series of experiments. First, they proved which structure of the fungi releases the toxin. Scientists had previously suspected that this task is performed by tiny balls that grow on the fungal hyphae like little lollipops and burst when touched. To test this, Lee and his team grew oyster mushrooms that lacked this structure, known as toxocysts. And indeed: the mutated oyster mushrooms without toxocysts were not able to kill nematodes.
Broad toxicity against nematodes
In the next step, the research team mechanically destroyed the toxocysts of wild-type oyster mushrooms and immediately placed C. elegans nematodes on the substrate. “We observed that in this case the nematodes were able to move freely in the fungal culture,” the researchers say. “The immediate loss of toxicity right after destroying the toxocysts gave us an indication that the compound could be volatile.” The researchers tested this hypothesis using a technique called gas chromatography-mass spectrometry. This makes it possible to identify volatile organic compounds. This is how they found out that the compound was 3-octanone, a volatile compound with eight carbon atoms that is also produced by plants such as lavender and rosemary, among others.
In the laboratory, the team tested how this substance, which is harmless to humans, affects roundworms. “We observed that 3-octanone paralyzed nematodes such as C. elegans and several other species at concentrations above 50 percent,” the researchers said. “This suggests that 3-octanone has broad toxicity against diverse species of nematodes.” When the nematodes came into contact with the venom, they lost their ability to move almost immediately. At the molecular level, the researchers observed a massive influx of calcium into the muscle and nerve cells of the nematodes. The calcium content also increased sharply in the mitochondria, the power plants of the cells, whereupon the mitochondria filled with water and burst. As a result, the cells of the nematodes perished and the animals died.
Oyster mushrooms for farming?
From the researchers’ point of view, these results not only provide interesting insights into the hunting strategy of oyster mushrooms, but can also possibly be used for agriculture. “Future studies examining how toxocyst development is regulated by environmental or physiological factors could provide strategies for using oyster mushrooms as an effective biocontrol agent against parasitic nematodes in agriculture,” the authors said. Since 3-octanone was less effective in the laboratory tests than the toxin of wild-type oyster mushrooms, they assume that the substance interacts with other organic compounds from the toxocysts in nature. The team intends to investigate what these might be in future studies.
Source: Ching-Han Lee (Academia Sinica, Taipei, Taiwan) et al., Science Advances, doi: 10.1126/sciadv.ade4809