A Minimal Model of Metabolism-Based Chemotaxis

Abstract

Since the pioneering work by Julius Adler in the 1960's, bacterial chemotaxis has been predominantly studied as metabolism-independent. All available simulation models of bacterial chemotaxis endorse this assumption. Recent studies have shown, however, that many metabolism-dependent chemotactic patterns occur in bacteria. We hereby present the simplest artificial protocell model capable of performing metabolism-based chemotaxis. The model serves as a proof of concept to show how even the simplest metabolism can sustain chemotactic patterns of varying sophistication. It also reproduces a set of phenomena that have recently attracted attention on bacterial chemotaxis and provides insights about alternative mechanisms that could instantiate them. We conclude that relaxing the metabolism-independent assumption provides important theoretical advances, forces us to rethink some established pre-conceptions and may help us better understand unexplored and poorly understood aspects of bacterial chemotaxis.

Author Summary

Traditionally, bacterial chemotaxis has been treated as metabolism-independent. Under this assumption, dedicated chemotaxis signalling pathways operate independently of metabolic processes. There is however, in various strains of bacteria, growing evidence of metabolism- dependent chemotaxis where metabolism modulates behavior. In this vein, we present the first model of metabolism-based chemotaxis that accomplishes chemotaxis without transmembrane receptors or signal transduction proteins, through the direct modulation of flagellar rotation by metabolite concentrations. The minimal model recreates chemotactic patterns found in bacteria, including: 1) chemotaxis towards metabolic resources and 2) away from metabolic inhibitors, 3) inhibition of chemotaxis in the presence of abundant resources, 4) cessation of chemotaxis to a resource due to inhibition of the metabolism of that resource, 5) sensitivity to metabolic and behavioral history and 6) integration of simultaneous complex environmental “stimuli”. The model demonstrates the substantial adaptability provided by the simple metabolism-based mechanism in the form of an ongoing, contextualized and integrative evaluation of the environment. Fumarate is identified as possibly playing a role in metabolism-based chemotaxis in bacteria, and some consequences of relaxing the metabolism-independent assumption are considered, causing us to reconsider the categorization of environmental compounds into “attractants” or “repellents” based solely on their binding properties.