Fungus farming leaf-cutter ants

29 January 2019

Interview with 

Koos Boomsma, University of Copenhagen

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An ant

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We depend upon our microbiomes, the populations of bacteria that live all over us, to keep us healthy. They assist us in digesting our dinner; they keep out other disease-causing microbes; and they even manufacture molecules that we can’t and which play an important role in many organs in our bodies, including even the brain. Some insects have gone further and developed an even closer relationship with their microbial passengers, as the University of Copenhagen’s Koos Boomsma explains to Chris Smith...

Koos - Well the research is about attine fungus-growing ants; and they're very special: they farm their own food in underground gardens, and that is almost everything they eat. These ants have been around for a very long time. They emerged shortly after the dinosaurs went extinct. So what we set out to do is actually look at the bacteria that live in their guts. We focused on a group that is called mollicutes: tiny bacteria without a cell wall. They're usually considered to be pathogens, but that didn't make sense to us because there were often millions inside a single ant that never looked sick. So we decided to get two of those genomes sequenced, because if you have that, you can usually infer a lot about what the functions.

Chris - So you can begin to ask questions about what these bugs are and where they might have come from?

Koos - Yes. So we had two sources of background material. One is that the Internet actually has lots of sequenced genomes of similar bacteria that just live inside other insects. So once you have genomes you can start making these comparisons. The other opportunity to that offered is actually to try and see what their closest relatives are, which gave us some very interesting pointers at where they may come from. And it turned out the two bacteria that we did end up sequencing had very different origins, even though they're in the same group of bacteria; and that one of them is basically findable throughout all the fungus-farming ants, whereas the other is exclusively found in the leaf cutter ants. And it quite intriguingly might have a close ancestor that is actually a symbiont that lives inside the leaves of plants, which is very interesting given that leaf cutter ants actually cut leaves to manure their fungus gardens.

Chris - So your hypothesis then would be that, way back in history when these ants first evolved, they were preying on plants - or interacting with plants - and they acquired these or very similar members of this bacterial family via that route, and they've since incorporated them into their microbiome?

Koos - Yes that is what it looks like. And they actually dominating the microbiome. One thing that we found these bacteria have special abilities to decompose chitin, which is very common in the cell walls of fungi and that is what these ants eat. Two other major things that we found is that both of the symbionts process a single amino acid: arginine. And, finally, that there was an important function of decomposing citrate.

Chris - Tell us about the arginine first; why is that important, and where's all the arginine coming from?

Koos - Well arginine is the amino acid that has most nitrogen and nitrogen is always important because that's what you need for making protein. So nitrogen is often a substance that limits growth. And a hallmark of this symbiosis,  when the ends became completely dependent on farming fungi for food, basically the hallmark of that is that the ants lost the ability to synthesise argenine, because the fungus was providing plenty. So the only kind of challenge that such a clever symbiotic swap may imply is that you later may sometimes get too much and you can't just give a complex amino acid back to your fungus garden when you defaecate on that - because that's what the ants do, they manure the fungus gardens with their own faeces - it is actually very clever if he can first return that to ammonia; and that is exactly what these bacteria - these molecutes - seem to be providing to the ants.

Chris - And what about the other two functions?

Koos - Well the fact that chitin is decomposed seemed obvious, because if you only eat fungus a lot of that will be relatively hard to digest fungal cell wall material. So if you have a bacterial symbiont in your gut that does that for you, that seems to be quite a clever acquisition. The final thing, citrate, is a function only found in the leaf cutting ant symbiont, not in the other one that is general for all the fungus growers. And citrate is something that you typically find in juices that you get when you start cutting fresh leaves, and the leaf cutter ants basically were ingesting - and which they probably couldn't really utilise - until they had a bacterial symbiont helping them to do that. The evolutionary less advanced fungus-growers don't cut fresh leaves - they live off dead plant material which they put on that fungus gardens - so they wouldn't necessarily have any use of having a bacterial symbiont that could handle citrate.

Chris - And do the ants acquire the symbiont when they are larvae? So when they're being fed and nurtured by workers is that when they pick it up?

Koos - Yes, as far as we've been able to reconstruct, when queens found new colonies they will obviously have some of these molecutes with them, and then any new ants that hatches from the pupa in the colony will be fed by her older sisters and acquire her complement of molecutes inoculation, which will then basically mean she in her own body can manage that symbiont as far as is required to be an optimal farmer of the fungus gardens...

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