Cell aspect ratio is a mechanical winning strategy in microbial competition

Abstract

ABSTRACTBacteria’s competition for nutrients and territory drives biofilm evolution (1–4). The factors determining the outcome of competition among diverse bacterial species have a broad impact on a wide range of pathological (5), environmental (6), and microbiome interactions (7). While motility-related traits (8–11) and specific molecular mechanisms (12, 13) have been identified as potential winning attributes in bacteria, a shared and universally conserved feature determining competition remains elusive. Here, we demonstrate that a simple morphological feature of individual bacteria, cell aspect ratio, provides a winning trait for the population. Using range expansion experiments (14), we show that relatively longer bacteria robustly conquer the expanding front, even when initially in minority. Using an agent-based model of dividing bacteria, we reveal that the takeover mechanism is their emergent collective alignment: groups of locally aligned bacteria form “nematic arms” bridging the central region of the colony to the expanding front. Once at the front, bacteria align parallel to it and block the access of shorter bacteria to nutrients and space. We confirm this observation with single-cell experiments and further generalise our findings by introducing a generic continuum model of alignment-dominated competition, explaining both experimental and cell-based model observations. Moreover, we extend our predictions to spherical range expansions (15) and confirm the competitive advantage of being longer, even though the effect is less pronounced than in surface-attached colonies. Our results uncover a simple, yet hitherto overlooked, mechanical mechanism determining the outcome of bacterial competition, which is potentially ubiquitous among various bacteria. With the current advances in genetic engineering, varying aspect ratios can work as a simple tunable mechanism for the on-demand setting of the outcome of bacterial competitions with widespread implications for biofilm control.