Spatial-temporal dynamics of a microbial cooperative behavior resistant to cheating

Hilary Monaco,Joao B Xavier,Maxime Deforet,Tiago Sereno,Bradford P Taylor,Kevin S Liu,Caleb C Reagor,Yanyan Chen

doi:10.1038/s41467-022-28321-9

Abstract

Much of our understanding of bacterial behavior stems from studies in liquid culture. In nature, however, bacteria frequently live in densely packed spatially-structured communities. How does spatial structure affect bacterial cooperative behaviors? In this work, we examine rhamnolipid production—a cooperative and virulent behavior of Pseudomonas aeruginosa. Here we show that, in striking contrast to well-mixed liquid culture, rhamnolipid gene expression in spatially-structured colonies is strongly associated with colony specific growth rate, and is impacted by perturbation with diffusible quorum signals. To interpret these findings, we construct a data-driven statistical inference model which captures a length-scale of bacterial interaction that develops over time. Finally, we find that perturbation of P. aeruginosa swarms with quorum signals preserves the cooperating genotype in competition, rather than creating opportunities for cheaters. Overall, our data demonstrate that the complex response to spatial localization is key to preserving bacterial cooperative behaviors.

Highlights

Much of our understanding of bacterial behavior stems from studies in liquid culture
The microenvironments inside bacterial communities are densely packed, dynamic, and highly competitive[8]. How can such cooperative traits persist despite intense competition when they carry a cost to cooperators? Understanding which factors favor selection for cooperative behaviors remains an open question in sociomicrobiology
We found rhlAB promoter activity to be low during periods of high specific growth rate as seen previously[22,28]

Summary

Introduction

Much of our understanding of bacterial behavior stems from studies in liquid culture. Recent work indicates that gene expression in spatially-structured systems, related to quorum signal communication, may differ from our liquid culture observations[29]. 2—Using this framework, we find that gene expression patterns in rhlAB promoter activity in the spatially-structured system differ from those previously characterized in liquid.

Results

Conclusion