Direct measurement of dynamic attractant gradients reveals breakdown of the Patlak-Keller-Segel chemotaxis model

Abstract

Chemotactic bacteria not only navigate chemical gradients, but also shape their environments by consuming and secreting attractants. Investigating how these processes influence the dynamics of bacterial populations has been challenging because of a lack of experimental methods for measuring spatial profiles of chemoattractants in real time. Here, we use a fluorescent sensor for aspartate to directly measure bacterially generated chemoattractant gradients during collective migration. Our measurements show that the standard Patlak-Keller-Segel model for collective chemotactic bacterial migration breaks down at high cell densities. To address this, we propose modifications to the model that consider the impact of cell density on bacterial chemotaxis and attractant consumption. With these changes, the model explains our experimental data across all cell densities, offering new insight into chemotactic dynamics. Our findings highlight the significance of considering cell density effects on bacterial behavior, and the potential for fluorescent metabolite sensors to shed light on the complex emergent dynamics of bacterial communities. SIGNIFICANCE STATEMENTDuring collective cellular processes, cells often dynamically shape and respond to their chemical environments. Our understanding of these processes is limited by the ability to measure these chemical profiles in real time. For example, the Patlak-Keller-Segel model has widely been used to describe collective chemotaxis towards self-generated gradients in various systems, albeit without direct verification. Here we used a biocompatible fluorescent protein sensor to directly observe attractant gradients created and chased by collectively-migrating bacteria. Doing so uncovered limitations of the standard chemotaxis model at high cell densities and allowed us to establish an improved model. Our work demonstrates the potential for fluorescent protein sensors to measure the spatiotemporal dynamics of chemical environments in cellular communities.