|Dead ants infected with Ophiocordyceps unilateralis|
(Tul.) Petch (1931)
Torrubia unilateralis Tul. (1865)
Ophiocordyceps unilateralis is an entomopathogenic fungus predominantly found in tropical forest ecosystems. In order to increase its own fitness O. unilateralis utilizes the evolutionary trait of an extended phenotype to manipulate the behavioral patterns of an infected formicidae, specifically Camponotus leonardi of the tribe of campotini. The infected ants leave their canopy nest and foraging trails, heading for the forest floor in search of an area with a temperature and humidity level that is suitable for fungal growth. The infected ant will then use its mandible to affix themselves to a major vein on the underside of a leaf and eventually die.
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 attach to the ant, eventually breaking through the exoskeleton using mechanical pressures and enzymes. Yeast stages of the fungus spread in the ant's body and presumably produce compounds that affect the ant's hemocoel and utilizes the evolutionary trait of an extended phenotype to manipulate the behavioral patterns exhibited by the ant. These infected ants begin to have irregularly spaced full body convolutions which sends them to the forest floor. 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. Once the mandibles of the ant are secured to the leaf vein, atrophy quickly sets in destroying the sarcomere connections in the muscle fibers, and reduces the mitochondria and sarcoplasmic reticula. The ant is no longer able to control the muscles of the mandible and will remain affixed here. This lockjaw trait is popularly known as the death grip, and is essential in the fungus's fitness.
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 at a mean height of 25.20 ± 2.46 cm above the forest floor, 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 meter. "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
- 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.
- "Ophiocordyceps unilateralis". MycoBank. International Mycological Association. Retrieved 2011-07-19.
- S., M., N., K., K., T., A., K., W., N., P., S., & ... J.J., L. (n.d). Life cycle, host range and temporal variation of Ophiocordyceps unilateralis/Hirsutella formicarum on Formicine ants. Journal Of Invertebrate Pathology, 111217-224. doi:10.1016/j.jip.2012.08.007
- Evans, H. C., Elliot, S. L., & Hughes, D. P. (2011). Hidden Diversity Behind the Zombie-Ant Fungus Ophiocordyceps unilateralis: Four New Species Described from Carpenter Ants in Minas Gerais, Brazil. Plos ONE, 6(3), 1-9. doi:10.1371/journal.pone.0017024
- Pontoppidan, Maj-Britt; Himaman, Winanda; Hywel-Jones, Nigel L.; Boomsma, Jacobus J.; Hughes, David P. (12 March 2009). "Graveyards on the move: The spatio-temporal distribution of dead Ophiocordyceps-infected ants". PLOS ONE 4 (3): e4835. doi:10.1371/journal.pone.0004835. PMID 19279680.
- Sung, Gi-Ho; Hywel-Jones, Nigel L.; Sung, Jae-Mo; Luangsa-Ard, J. Jennifer; Shrestha, Bhushan; Spatafora, Joseph W. (2007). "Phylogenetic classification of Cordyceps and the clavicipitaceous fungi". Studies in Mycology 57 (1): 5–59. doi:10.3114/sim.2007.57.01. PMID 18490993.
- Evans, Harry; Elliot, Simon; Hughes, David (September–October 2011). "Ophiocordyceps unilateralis – A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests?". Communicative Integrative Biology 4 (5): 598–602. doi:10.4161/cib.4.5.16721 (inactive 2014-01-13). PMC 3204140.
- Sample, Ian (18 August 2010). "'Zombie ants' controlled by parasitic fungus for 48m years". News » Science » Microbiology. The Guardian. Retrieved 2010-08-22.
- Evans, H., Elliot, S., & Hughes, D. (2011). Ophiocordyceps unilateralis: A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests?. Communicative & Integrative Biology, 4(5), 598-602. doi:10.4161/cib.4.5.16721
- Andersen, S. B., Gerritsma, S., Yusah, K. M., Mayntz, D., Hywel‐Jones, N. L., Billen, J., ... & Hughes, D. P. (2009). The life of a dead ant: the expression of an adaptive extended phenotype. The American Naturalist, 174(3), 424-433.
- Hughes, D. P., Andersen, S. B., Hywel-Jones, N. L., Himaman, W., Billen, J., & Boomsma, J. J. (2011). Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecology, 11(1), 13-22. doi:10.1186/1472-6785-11-13
- "Fossil Reveals 48-Million-Year History of Zombie Ants". Science Daily. 18 August 2010. Retrieved 2010-09-12.
- Hughes, David P.; Wappler, Torsten; Labandeira, Conrad C. (23 February 2011) [18 August 2010]. "Ancient death-grip leaf scars reveal ant fungal parasitism". Biology Letters (Royal Society) 7 (1): 67–70. doi:10.1098/rsbl.2010.0521. PMID 20719770.
- (2011), "Zombie Ants have fungus on the brain, new research reveals". Science Daily. Accessed on 2012-11-27.
- Attenborough, David. "Cordyceps: attack of the killer fungi". Planet Earth. BBC Worldwide. http://www.youtube.com/watch?v=XuKjBIBBAL8. Retrieved 4/21/13.
- Andersen, Sandra B.; Gerritsma, Sylvia; Yusah, Kalsum M.; Mayntz, David; Hywel‐Jones, Nigel L.; Billen, Johan; Boomsma, Jacobus J.; Hughes, David P. (September 2009). "The life of a dead ant: The expression of an adaptive extended phenotype". The American Naturalist 174 (3): 424–433. doi:10.1086/603640. JSTOR 10.1086/603640. PMID 19627240.
- Harmon, Katherine (31 July 2009). "Fungus makes zombie ants do all the work". Scientific American. Retrieved 2010-08-22.
- Xiao, Jian-Hui; Zhong, Jian-Jiang (2007). "Secondary metabolites from Cordyceps species and their antitumor activity studies". Recent Patents on Biotechnology 1 (2): 123–137. doi:10.2174/187220807780809454. PMID 19075836.
- P. Kittakoopa, J. Punyaa, P. Kongsaeree, Y. Lertwerawat, A. Jintasirikul, M. Tanticharoena, and Y. Thebtaranonth (1999), "Bioactive naphthoquinones from Cordyceps unilateralis" Phytochemistry, volume 52, issue 3, pages 453–457. doi:10.1016/S0031-9422(99)00272-1
- Wongsa, Patcharaporn; Tasanatai, Kanoksri; Watts, Patricia; Hywel-Jones, Nigel (August 2005). "Isolation and in vitro cultivation of the insect pathogenic fungus Cordyceps unilateralis". Mycological Research 109 (8): 936–940. doi:10.1017/S0953756205003321. PMID 16175796.
- Unagul, Panida; Wongsa, Patcharaporn; Kittakoop, Prasat; Intamas, Sutichai; Srikitikulchai, Prasert; Tanticharoen, Morakot (April 2005). "Production of red pigments by the insect pathogenic fungus Cordyceps unilateralis BCC 1869". Journal of Industrial Microbiology and Biotechnology 32 (4): 135–140. doi:10.1007/s10295-005-0213-6. PMID 15891934.
- "The Zombie-Ant Fungus Is Under Attack, Research Reveals". Pennsylvania State University. 2012-05-02. Retrieved 2013-03-04.
- Andersen, Sandra B.; Ferrari, Matthew; Evans, Harry C.; Elliot, Simon L.; Boomsma, Jacobus J.; Hughes, David P. (May 2, 2012). "Disease Dynamics in a Specialized Parasite of Ant Societies". PLOS ONE 7 (5): e36352. doi:10.1371/journal.pone.0036352.
- Hill; Kyle (2013-06-25). "The Fungus that Reduced Humanity to The Last of Us". Scientific American.
- Ophiocordyceps unilateralis at UniProt.org. Accessed on 2010-08-22.
- An Electronic Monograph of Cordyceps and Related Fungi