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Symbiotic Interactions

Introduction

Symbiosis can be defined as the association between dissimilar organisms in which benefit may accrue to both at least for a period during the association. Associations need not be static. In a few cases, the symbiotic phase may continue to a parasitic or commensal phase. The following are examples where symbiosis appears to continue for much of the life cycle of both organisms, and where the functional integration between partners is highly evolved.

Scale Insects and Fungi

Mutually beneficial interactions between insect and fungus can be viewed from the point of view of the partners or humans. A case of the former involves Septobasidial fungi (Basidiomycota) and scale insects. They form an association in which the insect relies on the fungus to provide protection from predators, parasites and pathogens. The fungus gains nutrients and a means of dispersal, and appears to rely on the insect absolutely.

cottony scale
Cottony scale on Podocarpus.

The fungus grows a tough cover over the colony of scale insects. The fungus also penetrates insects through natural openings forming haustoria LINK in the haemocoele of individuals. Insects continue to feed, providing a flow of nutrients to the fungus directly from the plant. Parasitised insects do not reproduce, and other, non-parasitised individuals enable the continuation of the insect, reproducing within the protection of the fungal shield.

The fungus releases a chemical attractant. Once detected, the insect associates with the fungus forming a colony. Some members of the colony become parasitised. Once the fungus has access to nutrients it spreads over the colony. The insect provides chemical signals that appear to modify the structure of the fungal covering. The fungal shield consists of a series of tunnels, apparently developed in response to the insects. In addition, the fungus is dispersed by scale insects carrying basidiospores from infested trees to uninfested trees.

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Leaf Cutter Ants, Termites and Fungi

Fungus-growing ants (Tribe Attini in the family Formicidae) obligately depend on the cultivation of a fungal mutualist for their nutrition. The tribe Attini has been divided into higher and lower groups. The higher Attine ants (the genera Atta and Acromyrmex) cultivate fungal gardens in their colony, using leaf material harvested from adjacent living plants. The fungus found in colonies of higher Attine ants is of the tribe Leucocoprinae in the family Lepiotiaceae.

The symbiosis has been well studied because of the damage ants can do to crops and forests. Found in the tropics of the Americas, Attine ants harvest leaf material from many different plant species, shred the material and feed it to their fungus garden in the ant colony. Each leaf fragment is inoculated with a fragment of fungus and then placed in the fungal garden. The garden consists of chewed leaf surrounded by a dense mycelium. The mycelium is characterised by formation of hyphae with swollen tips called staphylae. The staphylae are harvested by worker ants, held in the gut and subsequently fed to larvae or digested by the adult.

The lower Attine ants have smaller colonies, commonly among leaf litter. They feed their fungi on leaves, insects and other organic matter. The fungi of the lower ants appear to be polyphyletic. Interestingly, sequence analysis suggests that the more stable association between the higher group and Leucocoprinae is also the most ancient.


Diagram of an ant.

The fungus forms the majority of the nutrient for larvae, but is relatively unimportant for the adult. However, enzymes in the fungus may play a part in detoxifying or digesting the plant material obtained by the adult. Establishment of new colonies requires transport of mycelium by the queen (vertical transmission) as the fungus is thought to lack sporulation, though occasional basidiocarps may be seen associated with abandoned ant colonies.

Just as in laboratory culture, the fungus garden has a distinct chance of becoming contaminated by unsuitable fungi. Spores of a variety of fungi are common in air, and the ants will possible carry spores on their bodies as they move around their habitat. One fungus, Escovopsis is known to reduce an ant colony very rapidly. Interestingly, the ants of at least one group have a system minimising contamination. Leaf fragments are cleaned before inoculation. Spores licked from bodies and colony surfaces are stored in pouches on the body, and pellets discarded outside the colony. The mycelium is also constantly weeded, removing "foreign" fungi and bacteria. Waste in the nest is taken to a point downhill and away from the mouth of the colony. In addition, the workers that remove waste use an entrance separate from that used for other activities. These approaches reduce the chance of contamination, though heavily contaminated colonies are abandoned.

Interestingly, weeding and grooming are processes that require recognition of 'foreign" and useful symbionts. The recognition molecules or cues are unknown. It might be assumed that the cue is odorous as ants use olfactory cues for recognition. Fungi can produce various odours, and each species might have specific cues. However, any "foreign" organism able to mimic a useful symbiont would then be able to benefit from the cleansing and feeding provided to the fungus garden. Production of odoriferous cues remains to be examined in most fungi.

(Thanks to Alyson Ashe for allowing me to use her work in this section)

Termites and Fungi

The fungus Termitomyces (Tricholomataceae, Basidiomycota) forms similar, specific symbioses with termites in the Macrotermitinae, enabling the establishment of huge colonies in tropical Africa and Asia. In the "higher" termites, the fungus is carried by the queen (vertical transmission) of two species of termite to form new colonies. In the lower termites, horizontal transmission is most likely. Members of Termitomyces form basidiocarps and disperse spores horizontally. Thus termites may initiate colonies after selecting fungi from the environment.

The fungus is maintained in a fungal comb within the colony. Premasticated plant material is added to the young comb, and termites feed from the older parts of the comb.

Establishment of symbiosis with fungi by these social insects have enabled the insects to establish large, long-lived and complex colonies. With the symbiosis, the insects are able to occupy niches with abundant resources. The fungi have gained access to the resources and environments where they are artificially maintained.

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Endosymbionts of Arthropods

Microbes in their gastro intestinal tract (GIT) of many organisms aid in digestion LINK. The microbes are referred to as endosymbionts to distinguish them from symbionts that lack a tight association. Apart from the commensal fungi of the Trichomycetes, microbes including fungi are found in the GIT of a wide range of arthropods. LINK


Diagram of an arthropod.

The microbes are held in various ways. Some are a component of the fluid moving through the GIT. They may have some activity but this is difficult to determine. Others are held in specialised structures within the body indicating the coevolution of the association. The structures include specialised fermentation chambers, and ducts of gastric glands. Endosymbionts may also be held within cells of the epithelium of the gut, Malphigian tubules, or fat bodies. As these different associations are found across a wide range of insect taxa, it might be argued that the association is of considerable benefit to both partners.

The specific activity of fungi is difficult to differentiate from other microbes so the following will consider all microbes. The microbe gains nutrients and protection from the association. The microbe is also transferred from generation to generation of host by deliberate inoculation of eggs from specialised pouches of the insect. Presumably the microbe is ingested as the larvae eat through the shell on hatching.

In most cases, the benefit of the endosymbiont to the host is unknown. In the few cases examined, it appears that the fungus provides its host with nitrogen, which is recycled from ingesta. The microbes probably supply essential amino acids, vitamins and sterols. While some microbes probably have the capacity to digest cellulose, supplementary ingestion of microbial cellulases is likely to be sufficient to degrade the cellulose consumed by the host.

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Ambrosia Beetles, Bark Beetles and the Sirex Wood Wasp

A range of insects that are found in living trees utilise fungi they carry with them to partially digest the timber thus nourishing the larvae. The associations are symbiotic, in that the insect carries the fungus from tree to tree in specific pouches called mycangia, and the fungus digests the food for the insect.

wood rot
Wood rot fungi may be carried by tunneling insects.

Ambrosia Beetles (sub-family Platypodinae) and other related weevils have a highly developed association with a group of ascomycetous yeasts (including Ambrosiella, Ascoidea, Cephaloascus and Dipodascus). The adult insect carries fungi in mycangia, deep pockets in the outer cuticle of the body. The eggs are deposited along with fungi into holes bored into the timber. The fungus germinates and colonises the tunnels bored by the insect. When hatched, larvae feed from the fungus. This association is interesting because the fungi form ambrosia along the walls of the tunnel. Ambrosia are thin walled cells that sprout as a continuous layer from underlying continuous hyphae within the timber. A range of insects feed from the ambrosia, including the insects that inoculated the timber.

Bark beetles excavate tunnels through the inner bark. Adults and larvae feed on the phloem, and incidentally, any fungi that may be present. The fungi may be carried with the insects from tree to tree. Two pathogens are carried in this way. Both Ceratocystis and Ophiostoma form long-necked perithecia that exude sticky spores above the bark. These spores are collected accidentally and dispersed to other trees. LINK

pine
Pine in woodland

When the wood wasp Sirex noctilio arrived in Australia, it caused great concern. The insect is known to cause shoot deformation in Pinus radiata. Females bore into shoots and deposits eggs and the fungus Amylostereum areolatum. The fungus causes a white rot of the timber, and the rot spreads rapidly. The fungus digests cellulose and oxidises lignin. Newly hatched larvae feed on the fungus, and also utilise fungal cellulases to digest components of timber. As with Ambrosia weevils, spores of the fungus are carried by the adult female in mycangia, and they are deposited into timber during oviposition.

Ironically, a nematode Deladenus may also be carried with the partners. The nematode also feeds on the fungus. After contacting a larval wasp, the nematode colonises the wasp, in some cases, reducing their fecundity or in extreme cases, sterilising females. When females lay eggs, the fungus and nematode are transferred to the hole. The cycle is thus complete.

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Conclusion

A few fungi have evolved close functional and structural associations with insects and other arthropods. The associations are closely integrated and mutually beneficial. In each case, the fungus appears to be gaining access to organic energy, and in a few systems, the animal ensures close association by dispersing with the symbiont attached.

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Reference

Abe T, Bignell DE, Higashi M. (2000) Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer.

Hajek AE, Glare TR, O'Callahan M (eds). (2009) Use of microbes for control of invasive arthropods. Springer.

Lawrence JF and Milner RJ. 1996. Associations between Arthropods and Fungi. Fungi of Australia, Vol 1B, 137 – 202.

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