Ophiocordyceps unilateralis

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 parasitoid fungus that infects ants such as Camponotus leonardi, and alters their behavior in order to ensure the widespread distribution of its spores. This is a prime example of such a parasite.^[2]

Morphology

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.^[3][4]

Life cycle

Like other fungi pathogenic to insects in the Ophiocordyceps genus, O. unilateralis targets a specific host species; which is ideally the Camponotus leonardi ant, but has been known to parasitize other closely related species of ants with lesser degrees of host manipulation and reproductive success.^[2]

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 affects the ant's brain and change its behaviour by unknown mechanisms, causing the insect to climb up the stem of a plant and use its mandibles to secure itself to the plant. Infected ants bite the leaf veins with abnormal force, leaving telltale dumbbell-shaped marks. A search through plant fossil databases revealed similar marks on a fossil leaf from the Messel pit which is 48 million years old.^[5][6]

The fungus then kills the ant, and continues to grow as its mycelia invade more soft tissues and structurally fortify the ant's exoskeleton.^[2] More mycelia then sprout out of the ant, and securely anchor it to the plant substrate while secreting antimicrobials to ward off competition.^[2] 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.^[2]

The changes in the behavior of the infected ants are very specific, giving rise to the term zombie ants, and tuned for the benefit of the fungus. 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. 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".^[7] When the dead ants are repositioned in various other situations, further vegetative growth and sporulation either fails to occur or results in undersized and abnormal reproductive structures.^[8]

Geographic distribution

Panglobal habitation of tropical forests, including those in Africa, Brazil and Thailand.^[9]

Host impact

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.^[3][4]

Medicinal potential

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.^[10]

Six bioactive naphthoquinone derivatives isolated from O. unilateralis, namely

• erythrostominone
• deoxyerythrostominone
• 4-O-methyl erythrostominone|4-O-methyl erythrostominone
• epierythrostominol
• deoxyerythrostominol, and
• 3,5,8-trihydroxy-6-methoxy-2-(5-oxohexa-1,3-dienyl)-1,4-naphthoquinone

showed anti-malarial activity in vitro.^[11][12]

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.^[13]

References

1. ^ "Ophiocordyceps unilateralis (Tul.) Petch 1931". MycoBank. International Mycological Association. http://www.mycobank.org/MycoTaxo.aspx?Link=T&Rec=281145. Retrieved 2011-07-19. 
2. ^ ^{a b c d e} Ian Sample (Wednesday 18 August 2010). "Parasitic mind control fungus exists for 48m years". Parascientifica.com. http://www.sw-gm.com/index.php?t=5987. 
3. ^ ^{a b} Pontoppidan MB, Himaman W, Hywel-Jones NL, Boomsma JJ, Hughes DP. (12 March 2009). Dornhaus, Anna. ed. "Graveyards on the Move: The Spatio-Temporal Distribution of Dead Ophiocordyceps-Infected Ants". PLoS ONE 4 (3): e4835. Bibcode 2009PLoSO...4.4835P. doi:10.1371/journal.pone.0004835. ISSN 1932-6203. PMC 2652714. PMID 19279680. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=2652714. 
4. ^ ^{a b} Sung GH, Hywel-Jones NL, Sung JM, Luangsa-Ard JJ, Shrestha B,et al. (2007). "Phylogenetic classification of Cordyceps and the clavicipitaceous fungi". Studies in Mycology 57: 5–59. doi:10.3114/sim.2007.57.01. ISSN 0166-0616. PMC 2104736. PMID 18490993. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=2104736. 
5. ^ Staff reporters (18 August 2010). "Fossil Reveals 48-Million-Year History of Zombie Ants". www.sciencedaily.com. ScienceDaily LLC. http://www.sciencedaily.com/releases/2010/08/100818105730.htm. Retrieved 12 September 2010. 
6. ^ Hughes, David P.; Wappler, Torsten; Labandeira, Conrad C. (August 18, 2010). "Ancient death-grip leaf scars reveal ant–fungal parasitism". Biology Letters (The Royal Society) 6 (3): 67–70. doi:10.1098/rsbl.2010.0521. ISSN 1744-957X. PMC 3030878. PMID 20719770. http://rsbl.royalsocietypublishing.org/content/early/2010/08/16/rsbl.2010.0521. 
7. ^ Sample, Ian (18 August 2010). "'Zombie ants' controlled by parasitic fungus for 48m years". guardian.co.uk (Guardian Media Group). http://www.guardian.co.uk/science/2010/aug/18/zombie-carpenter-ant-fungus. Retrieved 2010-08-22. 
8. ^ Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL, Billen J, Boomsma JJ, Hughes DP. (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. ISSN 0003-0147. PMID 19627240. 
9. ^ Katherine, Harmon (31 July 2009). "Fungus Makes Zombie Ants Do All the Work". Scientific American. ISSN 0036-8733. http://www.scientificamerican.com/article.cfm?id=fungus-makes-zombie-ants. Retrieved 2010-08-22. 
10. ^ Xiao JH, Zhong JJ. (June 2007). "Secondary Metabolites from Cordyceps Species and Their Antitumor Activity Studies". Recent Patents on Biotechnology 1 (2): 123–137. doi:10.2174/187220807780809454. ISSN 1872-2083. PMID 19075836. http://www.ingentaconnect.com/content/ben/biot/2007/00000001/00000002/art00002. 
11. ^ Kittakoopa, P.; Punyaa, J.; Kongsaeree, P.; Lertwerawat, Y.; Jintasirikul, A.; Tanticharoena, M. and Thebtaranonth, Y. (October 1999). "Bioactive naphthoquinones from Cordyceps unilateralis". Phytochemistry 52 (3): 453–457. doi:10.1016/S0031-9422(99)00272-1. ISSN 0031-9422. http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6TH7-3X889NT-H&_user=10&_coverDate=10%2F31%2F1999&_rdoc=1&_fmt=high&_orig=search&_sort=d&_docanchor=&view=c&_acct=C000050221&_version=1&_urlVersion=0&_userid=10&md5=4234e873a4e2e5194249ec2a8515105e. 
12. ^ Wongsa P, Tasanatai K, Watts P, Hywel-Jones N (August 2005). "Isolation and in vitro cultivation of the insect pathogenic fungus Cordyceps unilateralis". Mycological Research 109 (Pt 8): 936–940. doi:10.1017/S0953756205003321. ISSN 0953-7562. PMID 16175796. http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B7XMR-4RS503Y-G&_user=10&_coverDate=08%2F31%2F2005&_rdoc=1&_fmt=high&_orig=search&_sort=d&_docanchor=&view=c&_acct=C000050221&_version=1&_urlVersion=0&_userid=10&md5=967a046938af39dfa67a73986d3cfdd4. 
13. ^ Unagul, P.; Wongsa, P.; Kittakoop, P.; Intamas, S.; Srikitikulchai, P. and Tanticharoen, M. (April 2005). "Production of red pigments by the insect pathogenic fungus Cordyceps unilateralis". Journal of Industrial Microbiology & Biotechnology 32 (4): 135–140. doi:10.1007/s10295-005-0213-6. ISSN 1367-5435. PMID 15891934. http://www.springerlink.com/content/p534744765456460/. 

External links

• "Ophiocordyceps unilateralis". UniProt.org. http://beta.uniprot.org/taxonomy/268505. Retrieved 2010-08-22. 
• An Electronic Monograph of Cordyceps and Related Fungi