Ophiocordyceps unilateralis

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Ophiocordyceps unilateralis
Dead ants infected with Ophiocordyceps unilateralis
Scientific classification
Kingdom: Fungi
Division: Ascomycota
Class: Sordariomycetes
Order: Hypocreales
Family: Ophiocordycipitaceae
Genus: Ophiocordyceps
Species: O. unilateralis
Binomial name
Ophiocordyceps unilateralis
(Tul.) Petch (1931)
Synonyms[1]

Torrubia unilateralis Tul. (1865)
Cordyceps unilateralis (Tul.) Sacc. (1883)

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.[2] This is a prime example of a parasitoid that alters the behavior of its host in order to ensure its own reproduction.[3] Possessed ants march to their death and the fungus lives inside the exoskeleton. [4]

Contents

Morphology [edit]

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.[5][6] The fungus infects ants, most known as the carpenter ants, in which the fungus creates a single stalk arising form 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.[7]

Life cycle [edit]

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.[3]

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 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.[8][9]

The fungus then kills the ant, and continues to grow as its hyphae invade more soft tissues and structurally fortify the ant's exoskeleton.[3] More mycelia then sprout out of the ant, and securely anchor it to the plant substrate while secreting antimicrobials to ward off competition.[3] 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.[3]

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.[10] 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. According to David Hughes, "You can find whole graveyards with 20 or 30 ants in a square metre. This fungus has been known to wipe out whole colonies of ants. [11] 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".[12] 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.[13]

Geographic distribution [edit]

The fungus occurs in tropical forests throughout the world, including those in Africa, Brazil, Thailand and Palau.[14]

Host impact [edit]

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.[5][6] 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 cadaver from microbial and scavenger attack.[15]

Medicinal potential [edit]

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.[16]

Six bioactive naphthoquinone derivatives have been isolated from O. unilateralis, namely

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.[19]

Anti-zombie-fungus fungus [edit]

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.[20][21]

References [edit]

  1. ^ "Ophiocordyceps unilateralis (Tul.) Petch 1931" at MycoBank. International Mycological Association. Accessed on 2011-07-19
  2. ^ Christine Dell'Amore (2012), "'Zombie Ant' fungus under attack". National Geographic (online). Accessed on 2012-11-28.
  3. ^ a b c d e Ian Sample (2010), "Parasitic mind control fungus exists for 48m years". 18 August 2010, at Parascientifica.com
  4. ^ BHANOO, SINDYA N. "Zombie-Ant Fungus Has Its Own Killer Fungus". NY Times. Retrieved 26 April 2013. 
  5. ^ a b M. B. Pontoppidan, W. Himaman, N. L. Hywel-Jones, J. J. Boomsma, D. P. Hughes (2009), "Graveyards on the move: The spatio-temporal distribution of dead Ophiocordyceps-infected ants". PLoS ONE, volume 4, issue 3, pages e4835. doi:10.1371/journal.pone.0004835 PMID 19279680.
  6. ^ a b G. H. Sung, N. L. Hywel-Jones, J. M. Sung, J. J. Luangsa-Ard, B. Shrestha, and others (2007). "Phylogenetic classification of Cordyceps and the clavicipitaceous fungi". Studies in Mycology, volume 57, pages 5-59, doi:10.3114/sim.2007.57.01, PMID 18490993
  7. ^ Evans, Harry C. "Ophiocordyceps unilateralis A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests?". Communicative and Integrative Biology. 
  8. ^ (2010) "Fossil Reveals 48-Million-Year History of Zombie Ants" Science Daily (online), 18 August 2010. Accessed on 2010-09-12
  9. ^ David P. Hughes, Torsten Wappler, Conrad C. Labandeira (2010), "Ancient death-grip leaf scars reveal ant fungal parasitism". Biology Letters of The Royal Society, volume 7, issue 1, pages 67-70. doi:10.1098/rsbl.2010.0521 PMID 20719770
  10. ^ (2011), "Zombie Ants have fungus on the brain, new research reveals". Science Daily. Accessed on 2012-11-27.
  11. ^ Attenborough, David. "Cordyceps: attack of the killer fungi - Planet Earth Attenborough BBC wildlife". BBC Worldwide. Retrieved 4/21/13. 
  12. ^ Ian Sample (2010), "'Zombie ants' controlled by parasitic fungus for 48m years". The Guardian (online), 18 August 2010. Accessed on 2010-08-22
  13. ^ S. B. Andersen, S. Gerritsma, K. M. Yusah, D. Mayntz, N. L. Hywel-Jones, J. Billen, J. J. Boomsma, D. P. Hughes (2009), "The life of a dead ant: The expression of an adaptive extended phenotype". The American Naturalist, volume 174, issue 3, pages 424-433 doi:10.1086/603640, PMID 19627240
  14. ^ Katherine Harmon (2009) "Fungus makes zombie ants do all the work". Scientific American (online), 31 July 2009. Accessed on 2010-08-22.
  15. ^ Evans, Harry; Simon Elliot,David Hughes (Sep-Oct 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. PMID PMC3204140. Retrieved 5 Apr 2013. 
  16. ^ J. H. Xiao, J. J. Zhong (2007), "Secondary metabolites from Cordyceps species and their antitumor activity studies". Recent Patents on Biotechnology, volume 1, issue 2, pages 123-137. doi:10.2174/187220807780809454 PMID 19075836
  17. ^ 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
  18. ^ P. Wongsa, K. Tasanatai, P. Watts, N. Hywel-Jones (2005) "Isolation and in vitro cultivation of the insect pathogenic fungus Cordyceps unilateralis". Mycological Research, volume 109, issue Pt 8, pages 936-940. doi:10.1017/S0953756205003321 PMID 16175796
  19. ^ P. Unagul, P. Wongsa, P. Kittakoop, S. Intamas, P. Srikitikulchai, and M. Tanticharoen (2005), "Production of red pigments by the insect pathogenic fungus Cordyceps unilateralis". Journal of Industrial Microbiology & Biotechnology, volume 32, issue 4, pages 135-140. doi:10.1007/s10295-005-0213-6 PMID 15891934
  20. ^ "The Zombie-Ant Fungus Is Under Attack, Research Reveals". Pennsylvania State University. 2012-05-02. Retrieved 2013-03-04. 
  21. ^ [1]
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