Coexisting with cheaters: Microbial exoenzyme production as a snowdrift
game model
Abstract
Cheating in microbial communities is often regarded as a precursor to a
“tragedy of the commons”, ultimately leading to over-exploitation by a
few species, and destabilisation of the community. However, this view
does not explain the ubiquity of cheaters in nature. Indeed, existing
evidence suggests that cheaters are not only evolutionarily and
ecologically inevitable, but also play important roles in communities,
like promoting cooperative behaviour. We developed a chemostat model
with two microbial species and a single, complex nutrient substrate. One
of the organisms, an enzyme producer, degrades the substrate, releasing
an essential and limiting resource that it can use both to grow and
produce more enzymes, but at a cost. The second organism, a cheater,
does not produce the enzyme but benefits from the diffused resource
produced by the other species, allowing it to benefit from the public
good, without contributing to it. We investigated evolutionarily stable
states of coexistence between the two organisms and described how enzyme
production rates and resource diffusion influence organism abundances.
We found that, in the long-term evolutionary scale, monocultures of the
producer drive themselves extinct because selection always favours
mutant invaders that invest less in enzyme production. However, the
presence of a cheater buffers this runaway selection process, preventing
extinction of the producer and allowing coexistence. Resource diffusion
rate controls cheater growth, preventing it from outcompeting the
producer. These results show that competition from cheaters can force
producers to maintain adequate enzyme production to sustain both itself
and the cheater. This is known in evolutionary game theory as a
“snowdrift game” – a metaphor describing a snow shoveler and a
cheater following in their clean tracks. We move further to show that
cheating can stabilise communities and possibly be a precursor to
cooperation, rather than extinction.