How to Keep your Fungal Garden Healthy

small-leafcutters

Leaf-cutter ants are absolutely fascinating little creatures. Found in North and South America, their colonies can contain up to 5 million ants and the queen of the colony can lay almost 30,000 eggs every day. These tiny workers have substantial impact on the ecological communities they live in: mixing the soil, selectively choosing which plants leaves to cut and which seeds to carry significantly modifies the environment they live in. And it is not for decorative purposes that they work so hard to bring those leaves back to their colonies (one piece of a leaf can weight up to 50 times the ant’s weight!). Leaf-cutter ants also belong to a group of fungus-growing ants, which, as their name implies, spend their time and resources on culturing fungi (process called fungiculture). Fungiculture has originated 50 million years ago and is an example of symbiosis, a mutually beneficial interaction between two or more organisms. Leaf-cutters bring the leaves back to the colony which provides a constant source of nutrition for their ‘fungal garden’ (this is the actual term used for the specialised space in the colony where the fungus is cultivated). As an added value the ants also take care of the fungal garden by cleaning it from any invading parasites as well as facilitating fungal spore dispersal. In return, ants eat the fungus, which is their primary food source (so it’s almost like a personal ant veggie garden).

A. Leaf-cutter ants B. Fungal garden in a wild  Leaf-cutter colony C. Dump part of a colony D. Leaf-cutter ant colony set up in a lab
A. Leaf-cutter ants
B. Fungal garden in a wild Leaf-cutter colony
C. Dump part of a colony
D. Leaf-cutter ant colony set up in a lab (from ref.1)

There are many aspects of this symbiotic relationship that are quite extraordinary. One of these is a question of how do ants maintain their fungal gardens healthy? As any gardener will tell, keeping your plants happy and flourishing is not an easy task. The constant in and out traffic from the ant colonies persistently brings spores of fungi, bacteria and other parasites into the fungal garden. Moreover, in densely populated societies of any form the threat of parasite spread do to congested living is quite substantial (as anyone who got a cold from a sick co-worker would attest). However, ants have acquired ingenious ways of dealing with this problem. Specifically, a fungus, known as Escovopsis, is a common fungal garden parasite that has a potential to overgrow the beneficial fungus maintained by the ants and ultimately lead to colony collapse. To prevent the growth of Escovopsis ants are constantly scavenging the garden for any Escovopsis spores. If an ant finds a spore it places it into an infrabuccal pocket, which is a structure in the oral cavity of an ant. Once the infrabuccal pocket is all filled up with the spores, the ant produces a small pellet from them and deposits it in the separate part of colony known as ‘the dump’ (everyone need a dumping ground I suppose…) (see figure above). And so, experiments with lab grown ant colonies have shown that if you dust the fungal garden with Escovopsis spores soon after you will see an increasing pile of these spore-pellets being deposited in the dump.

Actinomycete bacteria colony growing in the middle of the plate with Escovopsis fungus spreading along the edges. The clear no-grow area between the two is fungal growth inhibition zone caused by dentigerumycin released by the bacteria
Actinomycete bacteria colony growing in the middle of the plate with Escovopsis fungus spreading along the edges. The clear no-grow area between the two is fungal growth inhibition zone caused by dentigerumycin released by the bacteria (from ref.2)

Obviously, if ants would just move these spores out and left them so close to the garden there would still be quite a high chance of the spores being brought back but as it turns out these pellets no longer have any viable Escovopsis spores. How did that happen, I here you ask? Well, within the ant’s infrabuccal cavity grows a special bacterium. This bacterium (actinomycete) produces an antibiotic called dentigerumycin, which effectively sterilises the fungal spores essentially killing them (see figure above). Indeed, if you take the deposited spore pellet and seed it on the appropriate medium, you can culture the actinomycete bacteria but not the Escovopsis fungus from it. Interestingly, if the ant colony is dusted with UV-treated Escovopsis spores (UV treatment makes them unable to germinate) the ants don’t collect them and no spore pellets are made, which suggest that the tiny ant is somehow capable of distinguishing between viable and inviable spores, however, the mechanism for distinguishing the two is not yet understood.

The three-way symbiotic relationship (from ref.1)
The three-way symbiotic relationship (from ref.3)

I find this three way relationship absolutely astonishing:
If bacteria would not colonise the ants then they would not be able to keep parasites away, if parasites spread then the fungal garden gets smaller and if the garden fungus slowly dies then the leaf-cutters also die because there is not enough food available. With decreasing ant population the garden fungus also cannot survive because the supply of leaves is limited.

All of these organisms have to be in the right place at the right time for the symbiotic relationship to work. But then again, I suppose, that’s the way of nature- it makes things work… eventually… and it is the curiosity of a human which allows us to figure out how.

References
(1) Scott, Jarrod J., et al. “Microbial community structure of leaf-cutter ant fungus gardens and refuse dumps.” PLoS One 5.3 (2010): e9922.
(2) Oh, Dong-Chan, et al. “Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis.” Nature chemical biology 5.6 (2009): 391-393.
(3) Little, Ainslie EF, et al. “Defending against parasites: fungus-growing ants combine specialized behaviours and microbial symbionts to protect their fungus gardens.” Biology letters 2.1 (2006): 12-16.

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