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October 05, 2015 | By:  Sarah Jane Alger
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How Fungus Makes Ant Zombies

The parasitic fungus, Ophiocordyceps unilateralis sensu latu (O. unilateralis, for short), infects the brains of Carpenter ants, turning them into zombies that live and die for the sole purpose of helping the fungus thrive and reproduce. Under the influence of the fungus, zombie Carpenter ants leave their nests at an odd yet specific time, move randomly and convulsively, and climb up the north side of a plant to almost exactly 25 cm, where they bite the leaf vein. Once they bite the leaf, the muscles of their mandibles (mouth parts) deteriorate, causing lockjaw and fixing the ant victim in place while its legs kick and twitch. After a few hours, the movement stops as the fungus kills the ant, continues to grow throughout the victim's head, and then sprouts out of the back of the head. The fungus anchors itself to the plant and releases antimicrobial chemicals to protect itself and grows fruiting bodies from the ant's head to release its spores, spawning the next generation of fungus. O. unilateralis has been known to infect and wipe out entire Carpenter ant colonies, leaving dense aerial graveyards of ant carcasses in its wake.

A research team lead by David Hughes at Pennsylvania State University recently set out to explore how this fungal mind-invader accomplishes this gruesome feat through the use of modern genetic techniques. The researchers sequenced the genome of the O. unilateralis fungus and compared it with the genome of other related fungi. Of the 7831 genes that the researchers sequenced, they found several that code for toxins that are not commonly found in fungi. Some of these toxins are similar to cholera toxins (produced by diarrhea-causing bacteria) and others are similar to enterotoxins. The enterotoxins are a particularly interesting group of chemicals because they are known to screw up chemical communication, something that ants are heavily reliant upon.

The researchers then analyzed the activated genes in the heads of infected ants that had their jaws locked onto plants and compared these to the heads of uninfected ants. This tissue included a mix of ant brain, head muscles and fatty tissue as well as the parasitic fungus. They found that at the time that ants are locked onto their leaves but are still kicking, only about half of the cells in their head were their own: the rest were cells of their fungal invader. During this phase of zombie ant behavior, the parasitic fungus activates a set of genes that appear to be unique to O. unilateralis. For example, genes that affect neurotransmitters similar to serotonin, noradrenaline and dopamine were very active while the host ants display their odd zombie-like behaviors. Serotonin depletion in ants is known to prevent them from foraging properly. In other animals, disruption of these neurotransmitters can also cause hallucinations and muscle spasms. Thus, the fungus may be altering their host ants' behaviors in their favor through the manipulation of these neurotransmitter systems. Furthermore, two genes known to regulate circadian rhythms (daily activity patterns) are hyper-activated in zombie ants, which likely causes them to leave the nest at an odd time. Like other related mind-manipulating fungi, O. unilateralis secretes an enzyme that has been shown to increase activity in their insect hosts. This increased activity could be what causes the infected ants to leave their nests and crawl up a plant to their elevated places of death.

Once the ant victim bites down on the leaf that will become its aerial deathbed, the parasitic fungus activates a number of genes that cause the deterioration of the ants' jaw muscles, causing the lockjaw effect. It also activates a number of genes that suppress the ant's immune system, paving the way for the fungal cells to continue to grow and thrive throughout the ant's head tissues. A gene that is been shown to be overactive in patients with Alzheimer disease seems to play a role at this time as the fungal cells kill and displace the ant's brain cells.

Once the ants stop kicking and succumb to the fungus, a full 75% of the cells in their head are fungal cells. During this time, many genes in the fungal genome that relate to the digestion of the ant host, cell growth and reproduction kick into high gear as the fungus switches to a rapid growth phase to develop its reproductive stalk.

This genetic approach has provided tremendous insight to how the mind-manipulating fungus takes over the behavior of its ant host in such a dramatic and manipulative way. However, it may also reveal secrets for the development of drugs and other treatments for human health as well. For example, one set of fungal genes that are very active during the zombie ant behavior phase include lipocalin proteins. Lipocalins have been linked to a variety of functions, including metabolism, chemical communication, and the regulation of stress and the immune system. For these reasons, they are interesting candidates for drug discovery research. We have also seen the use of genes that may be relevant to neurodegenerative disorders, muscular degeneration, and behavioral disorders. We have a long history of using bioactive compounds produced by fungi for medicinal purposes. Because O. unilateralis secretes a number of unique compounds not produced by other fungi, this may open the door for some promising new research directions.


Further reading:
de Bekker, C., Ohm, R.A., Loreto, R.G., Sebastian, A., Albert, I., Merrow, M., Brachmann, A. and Hughes, D.P. Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation, BMC Genomics, 16:620, 1-23 (2015). DOI 10.1186/s12864-015-1812-x.

Image Credits:
"Ants biting the underside of leaves as a result of infection by O. unilateralis. The top panel shows the whole leaf with the dense surrounding vegetation in the background and the lower panel shows a close up view of dead ant attached to a leaf vein. The stroma of the fungus emerges from the back of the ant's head and the perithecia, from which spores are produced, grows from one side of this stroma, hence the species epithet. The photograph has been rotated 180 degrees to aid visualization." Ophiocordyceps unilateralis.png image and caption by David P. Hughes and Maj-Britt Pontoppidan at Wikimedia Commons.

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