Bacterial cartels at steady supply

Abstract

Metagenomics has revealed hundreds of bacterial species in almost all microbiota. In a few well-studied cases, bacterial communities have been observed to coordinate their metabolic fluxes. In principle, bacteria can divide tasks to reap the benefits of specialization, as in human economies. However, the benefits and stability of an economy of bacterial specialists are far from obvious. Here, we physically model the population dynamics of bacteria that compete for steadily supplied resources. Importantly, we explicitly model the metabolic fluxes yielding cellular biomass production under the constraint of a limited enzyme budget. In our framework, we find that population dynamics generally leads to the coexistence of different metabolic types, which satisfy an extended competitive exclusion principle (even allowing for adaptive mutation). We establish that these consortia act as cartels, whereby population dynamics pins down resource concentrations at values for which no other strategy can invade. Finally, we propose that at steady supply, cartels of competing strategies automatically yield maximum biomass, thereby achieving a collective optimum. SignificanceIn human economies, cartels are formed to avoid competition by controlling resource availability. Building on a physical model for resource-limited growth, we show that metabolic competition between bacteria similarly leads to the selection of cartels that control resource availability via population dynamics. Specifically, cartels avoid competition by pinning down resource concentrations at values for which no metabolic variant can outcompete the cartel's members. We propose that cartels also yield maximum biomass, constituting a microbial example of Adam Smith's "invisible hand" leading to collective optimal usage of resources. Our analysis illustrates how division of labor among distinct metabolic types can be predicted from optimization principles. These optimization principles, derived from transport-network theory, may provide a guide to understanding the division of labor in complex bacterial communities.

Paradoxes in Leaky Microbial Trade

“…This dynamical system is similar to the one Taillefumier et al [27] use to study coordination among bacterial populations when exposed to a diverse resource supply. In our situation, we have no externally supplied metabolites and do not allow cells to interconvert metabolites: all metabolites are immutable and produced by the cells themselves.…”