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

• Published in: Nature communications 2022-02, Vol.13 (1), p.721-721, Article 721
• Main Authors: Monaco, Hilary, Liu, Kevin S., Sereno, Tiago, Deforet, Maxime, Taylor, Bradford P., Chen, Yanyan, Reagor, Caleb C., Xavier, Joao B.
• Format: Article
• Language: English
• Subjects: 14/35; 14/56; 38/88; 38/90; 631/158/1144; 631/158/855; 631/326/41; Bacteria; Bacterial Proteins - genetics; Behavior; Biomass; Colonies; Colony Count, Microbial; Gene expression; Gene Expression Regulation, Bacterial; Genotypes; Glycolipids - genetics; Glycolipids - metabolism; Growth rate; Humanities and Social Sciences; Immunology; Life Sciences; Liquid culture; Localization; Locomotion; Mathematical models; Microbial Interactions - genetics; Microbial Interactions - physiology; Microorganisms; Models, Biological; multidisciplinary; Mutation; Optical Imaging; Perturbation; Promoter Regions, Genetic; Pseudomonas aeruginosa; Pseudomonas aeruginosa - genetics; Pseudomonas aeruginosa - growth & development; Pseudomonas aeruginosa - metabolism; Pseudomonas aeruginosa - physiology; Quorum Sensing; Science; Science (multidisciplinary); Spatial discrimination; Spatio-Temporal Analysis; Statistical inference; Stems
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-022-28321-9

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. Bacteria often live in densely packed, spatially-structured communities; however, much of our understanding of their behavior stems from studies in liquid culture. Here, Monaco et al. show how spatial structure and quorum sensing modulate a cooperative behavior in colonies of Pseudomonas aeruginosa .