|Dead ants infected with Ophiocordyceps unilateralis|
(Tul.) Petch (1931)
Torrubia unilateralis Tul. (1865)
Ophiocordyceps unilateralis is a parasitoidal fungus that infects ants such as Camponotus leonardi and alters their behavior. The ant falls from the tree where it normally lives, climbs on the stem of a plant, clamps its mandibles on a leaf and dies there, while the fungus consumes its tissues and grows outside it, releasing its spores. The infected ants are popularly known as zombie ants. This is a prime example of a parasitoid that alters the behavior of its host in order to ensure its own reproduction. Possessed ants march to their death and the fungus lives inside the exoskeleton.
The species can be identified at the end of its lifecycle by its reproductive structure, consisting of a wiry yet pliant darkly pigmented stroma stalk extending from the back of the deceased ant's head. The stalk has perithecia just below its tip. The fungus infects ants, most known as the carpenter ants, in which the fungus creates a single stalk arising from the dorsal neck region on which the sexual structures are borne horizontally, which creates the spores. Once infected with the fungus the ant will climb down from its normal habitat and bite down on the underside of a leaf. This is known as "the death grip" occurring in very precise locations.
Like other fungi pathogenic to insects in the Ophiocordyceps genus, O. unilateralis targets a specific host species, the Camponotus leonardi ant. However the fungus may parasitize other closely related species of ants with lesser degrees of host manipulation and reproductive success.
The fungus's spores enter the body of the insect likely through the cuticle by enzymatic activity, where they begin to consume the non-vital soft tissues. Yeast stages of the fungus spread in the ant's body and presumably produce compounds that affect the ant's brain and change its behaviour by currently unknown mechanisms. The insect climbs up the stem of a plant and uses its mandibles to secure itself to a leaf vein, with abnormal force, leaving dumbbell-shaped marks on it. A search through plant fossil databases revealed similar marks on a fossil leaf from the Messel Pit which is 48 million years old.
The fungus then kills the ant, and continues to grow as its hyphae invade more soft tissues and structurally fortify the ant's exoskeleton. More mycelia then sprout out of the ant, and securely anchor it to the plant substrate while secreting antimicrobials to ward off competition. When the fungus is ready to reproduce, its fruiting bodies grow from the ant's head and rupture, releasing the spores. This process takes 4 to 10 days.
The changes in the behavior of the infected ants are very specific, giving rise to the popular term "zombie ants", and tuned for the benefit of the fungus. The ants suffer from convulsions causing them to fall to the ground and preventing them from finding their way back to their canopy. The ants generally clamp to a leaf's vein about 25 cm above the ground, on the northern side of the plant, in an environment with 94–95% humidity and temperatures between 20 and 30 °C. Infections may lead to 20 to 30 dead ants per square metre. "Each time, they are on leaves that are a particular height off the ground and they have bitten into the main vein [of a leaf] before dying". When the dead ants are moved to other places and positions, further vegetative growth and sporulation either fails to occur or results in undersized and abnormal reproductive structures.
O. unilateralis has been known to destroy entire ant colonies. In response, ants have evolved the ability to sense that a member of the colony is infected; healthy ants will carry the dying one far away from the colony in order to avoid fungal spore exposure. Throughout the life cycle, there are unique challenges that must be met by equally unique metabolic activities. The fungal pathogen must attach securely to the arthropod exoskeleton and penetrate it—avoiding or suppressing host defenses—then, control the behavior of the host before killing it; and finally, it must protect the carcass from microbial and scavenger attack.
The Ophiocordyceps fungus contains various known and untapped bioactive metabolites, and is being investigated as a new source of natural drugs with immunomodulatory, antitumor, hypoglycemic and hypocholesterolemic functions.
Six bioactive naphthoquinone derivatives have been isolated from O. unilateralis, namely
- 4-O-methyl erythrostominone|4-O-methyl erythrostominone
- deoxyerythrostominol, and
- 3,5,8-trihydroxy-6-methoxy-2-(5-oxohexa-1,3-dienyl)-1,4-naphthoquinone showed anti-malarial activity in vitro.
There has also been research into the use of red naphthoquinone pigments made by O. unilateralis as a dye for food, cosmetic and pharmaceutical manufacturing processes.
O. unilateralis suffers from an unidentified fungal hyperparasite, reported in the lay press as the "anti-zombie-fungus fungus", that results in only 6–7% of sporangia being viable, limiting the damage O. unilateralis inflicts on ant colonies.
In popular culture
A fictitious variant of the fungus is featured in the game The Last of Us. The infection spreads to humanity and creates a zombie-like appearance/behavior, which causes the infected to become hostile and violent towards the non-infected.
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