Metabolic co-dependence gives rise to collective oscillations within biofilms

• Published in: Nature (London) 2015-07, Vol.523 (7562), p.550-554
• Main Authors: Liu, Jintao, Prindle, Arthur, Humphries, Jacqueline, Gabalda-Sagarra, Marçal, Asally, Munehiro, Lee, Dong-yeon D., Ly, San, Garcia-Ojalvo, Jordi, Süel, Gürol M.
• Format: Article
• Language: English
• Subjects: 13/62; 14/63; 631/326/41/2095; 631/326/46; 631/553/2693; 631/553/2717; Ammonium Compounds - metabolism; Ammonium Compounds - pharmacology; Analysis; Bacillus subtilis; Bacillus subtilis - cytology; Bacillus subtilis - drug effects; Bacillus subtilis - growth & development; Bacillus subtilis - metabolism; Bacteriology; Biofilms; Biofilms - drug effects; Biofilms - growth & development; Cell growth; Chronobiology Phenomena; Feedback, Physiological; Food; Genetic aspects; Humanities and Social Sciences; Metabolism; Metabolites; Microbial mats; Microfluidic Analytical Techniques; multidisciplinary; Nutrient availability; Physiological aspects; Science; Studies
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature14660

Cells that reside within a community can cooperate and also compete with each other for resources. It remains unclear how these opposing interactions are resolved at the population level. Here we investigate such an internal conflict within a microbial ( Bacillus subtilis ) biofilm community: cells in the biofilm periphery not only protect interior cells from external attack but also starve them through nutrient consumption. We discover that this conflict between protection and starvation is resolved through emergence of long-range metabolic co-dependence between peripheral and interior cells. As a result, biofilm growth halts periodically, increasing nutrient availability for the sheltered interior cells. We show that this collective oscillation in biofilm growth benefits the community in the event of a chemical attack. These findings indicate that oscillations support population-level conflict resolution by coordinating competing metabolic demands in space and time, suggesting new strategies to control biofilm growth. The emergence of long-range metabolic co-dependence within a biofilm drives oscillations in growth that resolve a social conflict between cooperation and competition, thereby increasing community-level fitness against chemical attack. Give-and-take within microbial biofilms During growth in a biofilm, cells at the periphery protect interior cells from external attack but can also starve them through nutrient consumption by the peripheral cells. Here Gürol Süel and colleagues find that this conflict between protection and starvation is resolved by the emergence of long-range metabolic co-dependence between cells at the periphery and the interior. In particular, they show in Bacillus subtilis biofilms that growth periodically halts, increasing the availability of nutrients to the sheltered interior cells, which in turn provide the metabolites necessary for growth at the periphery.