Leafcutter ants, fungi, and bacteria

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Introduction

This picture shows foraging ants carrying back cut sections of leaves. The volume of vegetation that they can carry and bring back is quite remarkable, as is the the size of their nest and the complexities lurking inside.
Picture taken from: http://www.asknature.org/strategy/6392180f395ab3f04ee8dd8b3ce632c4
Microorganisms often require a symbiotic relationship with other organisms in order to reproduce and survive. A fantastic example of a highly evolved example of the before mentioned symbiotic relationship can be shown through the interactions between leafcutter ants, fungi that are specific to the leafcutter nests, and a bacterium which is an antibiotic against the fungi's parasites. This relationship has previously been refered to as the "First Agriculture." The ants work as as a farmer who cultivates its crops (the fungus) trying to protect its goods from parasites in order to produce a healthy and bountiful crop. The fungal colonies once seemed to be free of any pests or parasites. This was thought to be because the ants were cared fro the fungas in such a diligent way taht they did not allow any parasites to enter and take hold. This theory was widely accepted until Cameron Currie took a closer look at what process was specifically keeping the nests parasite free. He noticed that when the ants were removed from the nest,the fungi was quickly taken over and destroyed. He was the first to find that the ants carried a white powdery bacteria on their abdomens that had antimicrobial properties. Without the ants, the parasitic mold could take over the fungus in the colony in a matter of days (Little, 2007).


Symbiotic Processes

A worker ant harvesting the fungus who is covered with the powdery white bacteria that helps the fungus stay parasite free.
Picture taken from: http://scienceblogs.com/notrocketscience/2009/11/leafcutter_ants_rely_on_bacteria_to_fertilise_their_fungus_g.php

Main Functions

A mutualistic symbiotic relationship is one where each partner contributes something special to the relationship and because of this they are both able to benefit. The fungus, ant, bacteria relationship is so special because of the intertwined actions and benefits that they each have. The fungus and the ants depend on each other for survival and one can not live without the other. The ants cultivate the fungus in its colonies from chewed up leaves and at the same time the fungus acts as the main food source for the ants.

Biological Interactions

The interaction begins when a queen attine ant leaves her original nest with a chunk of the Lepiotaceae fungus in her mouth, and colonizes a new nest. From there she can lay and the original piece of fungus can begin to be cultivated. To cultivate the fungus, the foraging ants go out and cut chunks out of leaves without ingesting any of the leave's toxic chemicals and bring them to the worker ants in the colony. Those ants take the leaves, chew them up, and use the pulp as a substrate for the fungus to grow on. This fungus is their main food source. The fungus could not survive without the ants, and the ants cant survive without the fungus.
But the ants have a special weapon in their arsenal for cultivating the fungi. They use the antibiotic producing actinomycete bacteria, that grows on the ants, as an antibiotic against outside sources of fungi and molds. This is how they keep their nest so clean and disease free. The antibiotic agent discourages the growth of fungi, except the specific fungi that the ants are growing. This is one reason why this interaction is so interesting, the different partners work specifically with each other in order to form a balanced and well functioning system that has lasted a very long time.

Fungi Growth

The leaves in the rain forest have toxic qualities in them which is supposed to deter herbivory. But the harvesting ants cut the leaves without ingesting any of the toxins and are able to bring the leaves back to the nest. There the leaves are given to worker ants which chew up the leaves in their mouths into a paste which becomes the food source for the fungus. The plant material is broken down through enzymes that break down the proteins and starches. Depending on the colony, the enzymes used can be slightly different promoting a complete plant break down or only a plant wall digestion. Because of the symbiotic relationship, the toxins in the leaves are able to be broken down by through enzymes from the fungi into needed sugars and proteins safe for the ant to consume.

Bacterial resistance to fungal parasites

To maintain a clean and healthy fungus colony, the ants have a bacteria on their exoskeleton which they use when cultivating the fungus. Some ants have this on their underbelly while ants that are in constant contact with the fungus are almost completely covered with the bacteria. This is an example of the complete evolutionary relationship bewteen the ant, the fungi, and the bacteria. The ants are able to use the bacteria, Pseudonocardia, with antibiotic qualities to fight against any invasive molds or fungi. This bacteria is similar to the bacterium which produces half the antibiotics made today. The antibiotic qualities allow it to specifically work with the fungus to inhibit the parasitic mold.

Unlike the ant, fungi, and bacteria symbiosis, present day antibiotics often produce resistant types of pathogens. It is thought that the ant colonies do not produce antibiotic resistant molds because of the high diversity of the bacteria and as the two evolve together the parasitic mold will not evolve a resistance.

Another method to cultivate only its native strain of Pseudonocardia is that the ant's feces contain incompatibility chemicals which select only for its resident fungus. There are also behavior cues which suggest that the ants physically pick out other types of fungus.

Environmental Implications

The millions of ants in the forests have a huge effect on the ecosystem. They consume 15-20% of fresh vegetation and up to 240 kg of dry leaves per year. These busy ants make up 86% of the total anthropod biomass. For such a small organism, it has a huge effect.

Nitrogen Fixation

Like any other garden, the ant's fungus garden needs nitrogen in an available form fit to be used by the microorganisms. Research has showed that the fungus garden in the ants' nest fixes nitrogen. This means that the fungus is taking atmospheric nitrogen and reducing the nitrogen to produce ammonium. Even after the nest uses the nitrogen that it needs, there is still a large amount of available nitrogen that can be entered into the surrounding system. This replenishes the nutrient poor tropical environment with an essential limiting nutrient (Pinto-Tomas, 2009).

Decomposition

The ants cut and collect a huge amount of forest vegetation each year. Needless to say, this has a huge effect on the tropical forest system. The decomposition effect of the ant-fungal-bacterial relationship needs to be considered when assessing the environmental impact of the relationship. When the plant material is brought to the nest, decomposition is aided by the ants chewing and initially breaking down the material, which can then be used as a substrate for the fungi. This speeds up decomposition in one place that would be spread out around the forest. Decomposition could also be hindered by the toxic qualities of the leaves leaving them inedible to other macro or micro invertebrates.
Decomposition is also aided by the previously mentioned nitrogen fixation process. Bringing nitrogen into the system helps to decrease the carbon to nitrogen ratio which speeds up the decomposition processes.

Niche

This is a split side view of an underground chamber where the fungus and the queen is housed. Every new colony starts with a small room like this one,which starts with a queen moving to a new place carrying the fungus in her mouth.
Picture taken from: http://laanitarainforestranch.com/pages/leafcutterants.htm

Habitat

The ant's nests are subterranean and can be found in mostly tropical areas including Costa Rica, Panama, and Argentina (Pinto-Tomas, 2009).

Nest Characteristics

Nests begin when a queen ant leaves one nest with a small amount of the fungus in her mouth and moves to a different area to start her own colony. Once a nest becomes established, the colonies can grow to have millions of ants in them.
These subterranean nests vary in sizes. They can be small with a single fungus growing "room" or can be multiple feet below ground with many different rooms and complex tunnels. Ants are also known as organized and clean insects. They have certain refuse dumps where the worker ants take the garbage and seclude it from the rest of the colony to decrease contamination.



Major Players

There are a total of five major players that interact with the leafcutter ants. There are the attine ants, their cultivated Lepiotaceae fungi, the parasitic fungal escovopsis parasites that feed on the cultivated fungi, and the latest partner; the black yeast found on the ants to help rid the colony of antagonistic invaders.

Ants

The group of ants that are LeafCutters belong to the tribe attini and their genera is Atta and acromyrmex These ants have been around for the better part of 50 million years. Interestingly, these ants are consume the largest amount of primary producers in the tropical rainforest areas which is not surprising considering their biomass is four times the amount of other invertebrates. World wide, these insects take up a third of the total insect biomass.

Fungi

Playing the role of both a decomposer and the primary food source for the Leafcutters, the fungi from the family Lepiotaceae is grown underground in the nests chambers by the worker ants. Other types of fungi can creep into the system, but are taken care of by the ants and are not allowed to keep surviving in the system.

Bacteria

Actinomycete bacteria are found in the underbellies of the worker ants. If the ants are in often close contact with the fungus, they tend to have more bacteria on them. This is because the bacteria has a special property that acts as antibiotic against other molds and fungi, except the ants' food source, the Lepiotaceae fungus.

Parasites

Battling against the ant's seemingly clean fungis' agriculture are parasites that would quickly take over the colony's fungus growth if not carefully weeded against. These can be competing molds or funguses that would come along and compete with the fungi for the delicious broken down vegetation. The ant's fungi cant survive against the invaders. Some of these parasites are refered to as escovopsis, and would feed on the fungus (Reynolds,2004).

Black Yeasts

There has recently been research conducted on a fourth fungal partner. One of the most interesting and only recently discovered partners is the antibiotic producing fungi Ascomycota; Phialophora. This is a black yeast that can be found on the cuticle of the ant and is used in a similar fashion in discouraging parasitic growth. This yeast has evolved with the ant-fungi symbiotic relationship and according to Little et al, the research into this partner shows how complicated and sophisticated this symbiotic partnership can be (Little, 2007). The fungus is prevalent in different geographical areas with the attine ants, and therefore the researchers concluded that the fungus is indeed a fourth symbiotic partner within the fungus, ant, bacterial mutualistic relationship (Little, 2007).

Current Research

Coevolution between attine ants and actinomycete bacteria

It has been the thought that the close relationship between the ant and the bacteria has caused the two to evolve together. But the study looks at if that is truly so. It concluded that the ant has probably evolved with the bacteria, but the bacteria has evolved independently. The study states that more research needs to be done on the reciprocality of the evolving partners (Dash, 2011).

Enzyme activity activity in different ant colonies

Ants have evolved into different sister clades. This research shows how the enzyme activity between lower and higher evolved colonies has changed. The study shows that higher evolved colonies contain more protein and starch digesting enzymes while those of lower clades have enzymes that just focus on partial degradation of the plant material (De Fine Licht, 2010).

Ant Genome

The complete ant genome has recently been mapped out. With that, their are multiple studies going on about the evolution of the ants with its symbiotic partners and other attributes of the ant. Especial focus is put on the antimicrobial properties of the bacteria (Ulrich, 2001).

Evolution and Competition

There are studies conducted to how the ant and its partners have evolved together and how they originally came to work together. This has led to studies on how the partners work to discourage different types of fungus and bacteria in interfering. This interference could lead to an instability within the network. Resistant pathogenic molds are also a source of research to see why they have not evolved over the years to take over the fungus (Ulrich, 2001).

References

Ask Nature, A project of the Biomimicry Institute. <http://www.asknature.org/strategy/6392180f395ab3f04ee8dd8b3ce632c4>

Dash, D., Mueller, U., Rabeling, C.,Rodrigues, A., 2008. "COEVOLUTION BETWEEN ATTINE ANTS AND ACTINOMYCETE BACTERIA: A REEVALUATION." Evolution 62. 11:2894-2912. Academic Search Premier. EBSCO. Web. 5 Apr. 2011.

De Fine Licht, H. H., Schiøtt, M., Mueller, U. G., & Boomsma, J. J. (2010). EVOLUTIONARY TRANSITIONS IN ENZYME ACTIVITY OF ANT FUNGUS GARDENS. Evolution, 64(7), 2055-2069.

Little, A., Currie, C. 2007. "Symbiotic complexity: discovery of a fifth symbiont in the attine ant-microbe symbiosis." PubMed.gov. 3(5):501-504

Reynolds, H. Currie, C. "Pathogenicity of Escovopsis weberi: The parasite of the attine ant-microbe symbiosis directly consumes the ant-cultivated fungus." 2004. Mycologia. 96(5): 955-959

Pinto-Tomas, A., Anderson, M., Suen, G., Stevensen, D., Chu, F., Cleland, W., Weimer, P., Currie, C. 2009. “Symbiotic Nitrogen Fixation in the Fungus Gardens of Leaf-Cutter Ants.” Science. 326: 1120-1123.

Ulrich, M., Schultz, T., Currie, C., Adams, R., Malloch, D. 2001. "The origin of the attin ant-fungus mutualism." 76:169-197

Edited by Katie Yi, a student of Angela Kent at the University of Illinois at Urbana-Champaign.