Who cheats and who eats? An evolutionary conundrum.

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Say what you will about our other vices, human beings did not invent cheating. Microbes have been doing it for billions of years. You see, for microbes, cheating can sometimes be an evolutionary advantage. And this can cause it to get out of hand really quickly.

Bacteria “cheat” by stealing each other’s lunch. They do it everywhere, all the time, and unwittingly. To understand why, we first need to consider how bacteria feed themselves.

Has it ever occurred to you what a convenience it is that most things we like eat are comparable to us in size? Probably not. But think about it for a second. Sure, some foods are quite a bit smaller than us (think nuts, berries and grains), while cows, bison and mastodons are certainly larger. But, in general, most things we eat are close enough to us in size that we can see, touch and handle them.

If this seems like a trivial observation, you may be surprised to learn it’s not always the case. Most of the things a bacteria would like to eat are thousands to millions of times too large for it to ingest. But bacteria have devised a clever way around this situation. They secrete enzymes, specialized proteins, out of their cells and into their environments. These so-called exoenzymes swim around chiseling bite sized fragments off anything they can: leaf scraps, insect remains, animal carcasses. Those fragments, sometimes a single molecule in size, can then be ingested by microbes and converted into energy.

Many bacteria rely entirely on exoenzymes for their food. However, enzymes are costly to build. All of the carbon and nutrients that go into making an enzyme could be spent elsewhere- on growth, reproduction, or cellular repair. Therefore, exoenzyme production is strictly regulated according to a simple rule anyone who has ever taken an introductory econ class will be familiar with: marginal revenues must exceed marginal costs. In other words, if you don’t get much benefit from that enzyme you just built, don’t build another one.

Here’s where cheating comes in. Exoenzymes are costly for the individual to produce, but they increase resource availability for the community. In econ-speak, exoenzymes are a public good. Once released into the “wild”, an enzyme is free to diffuse away from its producer. It can get stuck to a mineral, become inactivated by freezing or desiccation, or be eaten by another enzyme.  Given the risk associated with enzyme production, cheating can become an attractive alternative. Why produce enzymes yourself if you can enjoy free lunch thanks to your neighbors’ enzymes?

This type of microbial freeloading can become a major problem. The more cheaters are present in a population, the less return a producer will get on its’ exoenzymes. Too many cheaters, and suddenly it’s not worth anyone’s while to produce enzymes at all. Paradoxically, this leads to a situation where everyone’s starving, because no one can spare the resources needed to get food.

From a microbial perspective an exoenzyme is a tool for acquiring food. But on a global scale, exoenzymes serve a higher purpose. They are the engine that digests the dead, recycling carbon and nutrients back the living. They are the reason the surface of our planet is not piled high with the dead bodies of every living organism that ever was. Clearly, then, microbes have found ways of coping with the potentially debilitating effect of cheaters.

How, then, do microbial communities keep the cheaters in check? A group of microbial ecologists led by Dr. Steve Allison at the University of California, Irvine, devised a simple experiment using Pseudomonas fluorescens, a common soil bacteria, to investigate how and when cheating occurs. The study was published last week in the journal Frontiers in Microbiology.

The scientists first obtained two different strains of P. fluorescens. One strain had the genetic capacity to produce protease– a protein-decomposing enzyme. The other strain, a cheater, lacked the ability to produce the protease enzyme. The researchers created mixed cultures of these two strains and monitored the abundance of cheaters, producers, and protease over time.

When cheaters and producers were grown in 50/50 mixed cultures, protease activity declined to near zero. Rampant cheating apparently deterred everyone from making protease. More surprisingly, in cultures that contained only protease producers, enzyme activity still declined to near zero. Why? In an environment full of enzyme producers, cheaters have a selective advantage because they can get a free lunch. It’s possible that a genetic mutation resulting in an inability to produce protease- a cheater mutation- swept through the population.

So, given that cheaters cheat, and producers become cheaters who then cheat, how is it that microbial decomposition hasn’t ground to a halt? The answer, it turns out, may lie in the structure of the microbial environment. The experiments I just described were performed in liquid cultures. In liquid, enzymes move about freely via diffusion. The result is a cheater’s paradise, an environment where resources are abundant everywhere. At least for a short while.

But what about in a more structured environment, like soil? In soil, bacteria and enzymes adhere to solid particles. Depending on moisture levels, diffusion in soil can be rapid or very slow. If a producer’s exoenzymes stay close to home, they are more likely to provide their maker with benefits. In this case, the producers may actually have incentive to continue making enzymes. To test this idea, the researchers repeated their experiment, only this time, they grew P. fluorescens on solid agar in petri dishes. The results were quite different. Cheaters did not sweep the population. Instead, populations remained a patchwork of producers and cheaters.

In spite of its simplicity, this experiment has a profound implication for our understanding of microbial ecology. It demonstrates that environments with greater spatial structure favor a diversity of life strategies. In other words, increased environmental heterogeneity facilitates coexistence.

This finding is not unique to microbial ecology- we see a similar principle playing out across much larger scales. The introduction of invasive plants and animals to new ecosystems represents a breakdown of spatial boundaries; this results in the mixing of once-separate communities. We need only go to a kudzu-ridden forest in the Southern US, or read scifi-like stories of the cane toad devastation in Australia, to see for ourselves the link between spatial isolation and diversity. When populations are separate, they experience unique environmental challenges, leading to diverse adaptations and evolution. When systems become too mixed, diversity can lose out to a lower common denominator: who can hoard the most resources, grow and reproduce the fastest.

Ultimately, as systems become too well-mixed, too homogenous, they grow vulnerable to collapse. Remember, if everyone’s a cheater, no one eats.

ResearchBlogging.org
Allison, S., Lu, L., Kent, A., & Martiny, A. (2014). Extracellular enzyme production and cheating in Pseudomonas fluorescens depend on diffusion rates Frontiers in Microbiology, 5 DOI: 10.3389/fmicb.2014.00169

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