Friday, 30 June 2017

Fungus, parasites, and witches, oh my!

Figure 1: Festuca grass. Sometimes livestock that ingest Festuca or certain other grasses can cause them to have symptoms akin to extreme drunkenness: stumbling, disorientation, and paralysis.
Imagine a an old wild west town having its bank robbed. Two outlaws are running out of the bank, firing pistols into the morning sky and jumping on their horses while townsfolk are running to get the sheriff. A cross country pursuit begins: horses racing across the grassy prairie as the outlaws try to reach their hideout. At a river crossing one outlaw ties up his horse while helping the other cross. Later, his horse is stumbling and can't walk straight, finally, it lays down, hind legs paralyzed! The outlaws continue on one horse, but with two riders it moves more slowly and they are caught by the sheriff.

Ingesting festuca and other grasses can cause toxicosis - Unknown to the outlaws in the story above, while they crossed the river the waiting horse munched on a species of grass in the Festuca genus (Fig. 1). These grasses are well-known for causing toxicosis in grazing animals, leading to shaking or trembling, partial paralysis, and in some cases death. Today: the chemistry of these toxins.

Figure 2: Fungus produces ergot alkaloids. Plant scientists and mycologists have discovered that the drunkenness effects are due to toxins produced produced not by the plant, but by a fungus that lives inside some plants. Left: isolated fungus growing in a petri dish (top), microscope images of isolated endophytic fungus (bottom). Photo from Cabral et al. [1] Right: the basic chemical structure of ergot alkaloids.
Fungal endophytes produce toxins - Researchers tried to grow some toxicosis-causing plants in sterile, laboratory conditions to study their properties, but were surprised when, in addition to a plant growing, a large amount of fungus also grew along with the plant! They were able to isolate the fungus (Fig. 2, left), and after some tests, it became clear that it is not actually the plants that produce the toxins, but the fungus that lives inside the plant. In exchange for poisoning any attacking herbivore, the plant allows the fungus to live inside its walls, making the fungus an endophyte (endo=inside, phyte=grower). The fungus obliges by producing ergot toxins (Fig. 2, right), complicated molecules that belong to the class of chemicals called alkaloids (alkaloids contain at least one nitrogen atom, for example, caffeine and nicotine).

Colonies of fungal endophytes are transferred to plant offspring - In a another amazing twist, scientists found that a small amount of the fungus is stored inside the plant's seeds so that when new plants start growing, they already have a fungus colony inside them, ready to defend the plant as soon as the seed germinates. Overall, plants that host the fungus have an advantage in grazing fields. This advantage is so substantial that parasitic plants growing on roots of Festuca have evolved to steal some of the ergot toxins to protect themselves from herbivores as well.

Figure 3: Rye with visible endophyte fungus. Some crops can also host fungal endophytes, which can cause terrible symptoms in people who ingest them.
Ergot alkaloids can also affect humans - In addition to affecting grazing animals, the ergot alkaloids produced by fungal endophytes can also affect humans. If a human has a long-term diet that consists mainly of a grain containing a toxin-producing endophyte, alarming symptoms such as convulsions, itching, psychosis, and peeling skin can appear. Some scientists and historians have argued that ergot alkaloids were one cause of the Salem witch trials! The symptoms caused by ergot poisoning match those reported at the trials, and the townspeople ate lots of rye grown in a climatic region that would support the fungus (Fig. 3). Still, this idea is somewhat debated because several historians think Salem residents would have known of and recognized ergot poisoning.

Fungal endophytes in biotechnology - Whether or not fungal toxins played a role in the Salem witch trials, they will almost certainly play a role in the future of agriculture. Scientists are working on better understanding the nature of the relationship between the fungus and its host. So far they have found that, for example, fungal endophytes assist the plant in acquiring nitrogen from the soil [2], and that they help plants tolerate very hot environments [3]. These results suggest that we could increase the heat tolerance of our crops and decrease their need for fertilizer if we could introduce them to a fungal endophyte that the worked together with the plant in nitrogen acquisition and heat tolerance, but didn't produce toxins. This would decrease the environmental impacts of our agricultural system (fewer fertilizer applications) and make it more secure (less susceptible to extreme heat). Go crop science!

[1] Cabral, Daniel, et al. "Evidence supporting the occurrence of a new species of endophyte in some South American grasses." Mycologia (1999): 315-325.
[2] Behie, S. W., P. M. Zelisko, and M. J. Bidochka. "Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants." Science 336.6088 (2012): 1576-1577.
[3] Redman, Regina S., et al. "Thermotolerance generated by plant/fungal symbiosis." Science 298.5598 (2002): 1581-1581.