Ophiocordyceps unilateralis

A Microbial Biorealm page on the genus Ophiocordyceps unilateralis

Classification

| Fungi | Ascomycota | Sordariomycetes | Hypocreales | Ophiocordycipitaceae | Ophiocordyceps | O. unilateralis | Ophiocordyceps unilateralis

Description and Significance

Ophiocordyceps unilateralis (Ascomycota: Hypocreales) is a specialized fungal parasite that infects, manipulates and kills formicine ants, predominantly in tropical forest ecosystems. It specifically infects Camponotus leonardi of the tribe of campotini [3Evans, 2Hughes].

Worker ants are infected during foraging when the fungal spores attach to their cuticles [Hughes]. Germination and then penetration through the cuticle leads to rapid infection inside the host body [1Van, 2Hughes]. Once infected the ants will climb down from their natural habitats on rainforest tree and relocate to 25 cm off the ground under leaves where the temperature is low and humidity is high. Fungal reproduction is only possible after a stalk is grown out of the host’s head by propulsion of spores out from its fruiting bodies [3Evans]. Spores of O. unilateralis are actively discharged and dispersed over short distances, creating an infectious “killing field” of ∼1 m2 below the dead host (N. L. Hywel-Jones, unpublished data).

Fungal manipulation of an ant host’s mouthparts was found on a 48 million year old single leaf of the dicotyledonous plant host Byttnertiopsis daphnogenes from Messel in Northern Germany [4Hughes]. The close modern parallel for this distinctive type of leaf damage is the death grip of some fungus-infected carpenter ants such as the fungus O. unilateralis which adaptively manipulates worker ants of C. leonardi to bite along major veins of leaves in Thai tropical forests. This is the oldest evidence of parasites manipulating the behaviour of their hosts and suggests that the specialized interaction is relatively ancient rather than newly acquired[5].

Due to the increased amount of research on Ophiocordyceps in recent years, the name Ophiocordyceps unilateralis is often extended to Ophiocordyceps unilateralis sensu lato to indicate that the taxonomic system for this species is currently in flux [2Hughes] and will change as the genus and species characteristics become more defined.

Genome Structure

The genome of this organism is not sequenced entirely, although major enzymes such as RNA polymerases have been sequenced. Four polyketide synthase (PKS) genes have been found in O. unilateralis (Amnuaykanjanasin et al). PKS enzymes synthesize polyketide proteins, which have proven to be novel antibiotics, antifungal agents, and even cholesterol lowering agents (Amnuaykanjanasin et al). The genome obviously contains genes that encode for the very different life stages of the organism, from the yeast-like phase, to the mycelium phase, to the stalk formation (described in greater detail under cell structure and metabolism). More research is clearly needed in this area, as having the genome sequenced would further the knowledge of fungal parasite-host interactions that most likely happen pre-translationally (Evans et al). These pre-translational mechanisms are thought to involve silencing RNAs (Evans et al).

Cell Structure and Metabolism

There are three distinct phases of life for Ophiocordyceps unilateralis. The first is ascospore formation and germination, where ascospores are deposited on the hopeless ants and a projection called a germ tube goes into the insect (Wongsa et al). The ascospores are around 20-100 um in length, and skinny. The second phase is the yeast-like phase, where eventually a mycelium is made (Wongsa et al). The cells start off looking like individual yeast cells, which then come together to branch out, forming the mycelium (a common structure among fungi). The third phase involves penetration of the insect's cuticle by the newly formed stalk to sporulate and begin the process of infecting more ants (Wongsa et al).

As O. unilateralis is an entomopathogenic fungus, it's metabolism involves cellular processes based on the decomposition of the ant's body. The exoskeleton remains intact, however the innards of the ant are eventually consumed by the infection of the O. unilateralis yeast-like cell phase.

Ecology

Ophiocordyceps unilateralis have a pan-tropical distribution. They utilize as their hosts the local carpenter ant species, all of which fall within the tribe Camponotini (which include the genera Camponotus, Polyrachis, and Echinopla) . O. unilateralis is very ecologically driven, with the parasite specializing in specific host species depending on what is common to the area. It has recently been discovered that O. unilateralis has evolved to be especially effective against ants of the genus Camponotus (citation). Other sub species of O. unilateralis have been found that specialize in other genera of carpenter ants, leading scientists to push for a re-evaluation of the naming system for O. unilateralis s.l..

In the tropical forests, the host ants typically reside in the canopy. However, O. unilateralis is remarkably consistent in establishing itself at about 25cm above the forest floor (citation) on the underside of leafs. Though the reasoning behind this location is not entirely clear, researchers believe that the location prevents it from being washed away, the height gives it enough clearance to disperse the spores over a wide area, and the location on the underside of the leaf protects it from the elements.

Pathology

Test photo

(how it enters the host)

After O. unilateralis causes the mandibles of the ant to close upon the leaf vein, it begins to atrophy the striated muscle by destroying the sarcomere connections in the muscle fibers, as well as reducing the density of mitochondria and sarcoplasmic reticula (hughes behavioral mechanisms). The reduction in mitochondria lowers the amount of energy available to the mandible muscles and eliminates the ability for the muscle fibers to relax and contract, resulting in the permanent closure of the mandibles on the leaf vein (known as the death grip). This action is essential in ensuring that O. unilateralis remains at the proper height above the forest floor for the next steps of fungal development and spore release. Within 24 hours of death, hyphae are seen growing from a number of areas on the ant. Hyphae that protrude from the tarsae of the ants function to secure the ant to the leaf. As the hyphae begin to collect and mass together, stroma can be seen forming at the intersegmental membrane at the base of the ant’s head around the 2 day mark.

(stroma development and spore release mechanisms)

Current Research

In 2011, Hughes et al. studied the behavioral and morphological mechanisms of the fungus O. unilateralis (Hughes et al., 2011). For instance, countless hours of observation of the infected ants' walking patterns resulted in an observed random walking pattern as the research team had predicted, instead of a directed walk (Hughes et al., 2011). We now have a better understanding than before about the advanced and complex morphological and behavioral mechanisms that happen inside the ant while it is becoming a zombie, there is still much more to know about how the fungus O. unilateralis interacts with ant neurons on the molecular level. Genetic analysis should be done to first understand which proteins of the fungus are interacting with which genes of the ant genome (Hughes et al., 2011).

Current research is being done on the possibility that the organism could contain novel chemicals of medicinal use to humans. One of the more interesting recent findings was the presence of anti-malarial naphthoquinones within the organism (citation needed).

Cool Factor

By far the most interesting fact about the organism O. unilateralis is that it has the ability to take the body of an ant captive, turning it into a so-called "zombie ant" and manipulating its psychomotor functions via the release of toxins.

References

1. Van Pelt A: The occurrence of a Cordyceps on the ant Camponotus pennsylvanicus (De Geer) in the Highlands, N.C. region. Journal of the Tennesee Academy of Sciences 1958, 33(120-122).

2. Hughes DP, Evans HC, Hywel-Jones NL, Boomsma JJ, Armitage SAO: Novel fungal disease in complex leaf-cutting ant societies. Ecological Entomology 2009, 34(2):214-220.

3. Evans HC, Samson RA: Cordyceps species and their anamorphs pathogenic on ants (Formicidae) in tropical forest ecosystems. II. The Camponotus (Formicinae) complex. Transactions of the British Mycolocical Society 1984, 82:127-150.

4. Hughes, David P., Torsten Wappler, and Conrad C. Labandiera. "Ancient Death-grip Leaf Scars Reveal Ant-fungal Parasitism." Biology Letters (2010).

5. http://www.physorg.com/news201343671.html

Wongsa P, Tasanatai K, Watts P, Hywel-Jones N (2005) Isolation and in vitro cultivation of the insect pathogenic fungus Cordyceps unilateralis. Mycol Res 109:936–940.

Amnuaykanjanasin A, Phonghanpot S, Sengpanich N, Cheevadhana- rak S, Tanticharoen M (2009) Insect-specific polyketide syn- thases (PKSs), potential PKS-nonribosomal peptide synthetase hybrids, and novel PKS clades in tropical fungi. Appl Environ Microbiol 75(11):3721–3732.

http://www.biomedcentral.com/1472-6785/11/13/