The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies

Abstract

First principles of thermodynamics imply that metabolic pathways are faced with a trade-off between the rate and yield of ATP production. Simple evolutionary models argue that this trade-off generates a fundamental social conflict in microbial populations: average fitness in a population is highest if all individuals exploit common resources efficiently, but individual reproductive rate is maximized by consuming common resources at the highest possible rate, a scenario known as the tragedy of the commons. In this paper, I review studies that have addressed two key questions: What is the evidence that the rate-yield trade-off is an evolutionary constraint on metabolic pathways? And, if so, what determines evolutionary outcome of the conflicts generated by this trade-off? Comparative studies and microbial experiments provide evidence that the rate-yield trade-off is an evolutionary constraint that is driven by thermodynamic constraints that are common to all metabolic pathways and pathway-specific constraints that reflect the evolutionary history of populations. Microbial selection experiments show that the evolutionary consequences of this trade-off depend on both kin selection and biochemical constraints. In wellmixed populations with low relatedness, genotypes with rapid and efficient metabolism can coexist as a result of negative frequency-dependent selection generated by density-dependent biochemical costs of rapid metabolism. Kin selection can promote the maintenance of efficient metabolism in structured populations with high relatedness by ensuring that genotypes with efficient metabolic pathways gain an indirect fitness benefit from their competitive restraint. I conclude by suggesting avenues for future research and by discussing the broader implications of this work for microbial social evolution.

High bacterial carbon demand and low growth efficiency at a tropical hypereutrophic estuary: importance of dissolved organic matter remineralization

“…Warmer conditions enhance metabolic rates (BROWN et al, 2004), which also leads to higher energetic loss (MACLEAN, 2008;PFEIFFER et al, 2001). Therefore, water temperatures are often directly correlated to bacterial production and respiration (JIMENEZ-MERCADO et al, 2007;KIRCHMAN et al, 2005;POMEROY et al, 1995;RAYMOND;BAUER, 2000; SAMPOU; KEMP, 1994; SHIAH; DUCKLOW, 1994).…”

A critical view of metabolic network adaptations

“…On the basis of thermodynamic (and partly experimental, see MacLean, 2008;Novak et al, 2006) arguments, a trade-off between yield and rate in ATP production was shown theoretically to lead to a "tragedy of the commons" (MacLean, 2008;Pfeiffer et al, 2001). The basic idea is that organisms have two options: either convert substrate into biomass efficiently, but slowly, or consume the substrate fast with concomitant fast growth, but inefficiently.…”

Dynamics in the mixed microbial concourse

“…Defector strains, which fail to pay the cost of cooperation but receive the benefits, may exhibit higher fitness and quickly dominate the population. A variety of mechanisms exist to circumvent this game-theoretical constraint and allow cooperative phenotypes to thrive (Brännströ m and Dieckmann 2005;Nowak 2006;MacLean 2008;Chuang et al 2010).…”