Nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation

• Published in: Nature communications Vol. 8; no. 1; pp. 230 - 8
• Main Authors: Sexton, D. Joseph, Schuster, Martin
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 10.08.2017; Nature Publishing Group; Nature Portfolio
• Subjects: 631/326/2565/855; 631/326/41/1969/2180; 631/326/41/2095; Bacteria; Bacteria - growth & development; Bacteria - metabolism; Behavior; Biological Transport; Biomass; Biosynthesis; Carbon; Carbon - analysis; Carbon - metabolism; Coculture Techniques; Cooperation; Costs; Culture Media - chemistry; Culture Media - metabolism; Fitness; Genomes; Humanities and Social Sciences; Iron; Metabolism; Metabolites; Models, Biological; multidisciplinary; Nitrogen; Nutrients; Peptides; Phosphorus - analysis; Phosphorus - metabolism; Physical fitness; Pseudomonas aeruginosa; Pseudomonas aeruginosa - genetics; Pseudomonas aeruginosa - growth & development; Pseudomonas aeruginosa - metabolism; Pyoverdines; Science; Science (multidisciplinary); Secretion; Siderophores - metabolism
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-017-00222-2

Cooperative behaviors provide a collective benefit, but are considered costly for the individual. Here, we report that these costs vary dramatically in different contexts and have opposing effects on the selection for non-cooperating cheaters. We investigate a prominent example of bacterial cooperation, the secretion of the peptide siderophore pyoverdine by Pseudomonas aeruginosa , under different nutrient-limiting conditions. Using metabolic modeling, we show that pyoverdine incurs a fitness cost only when its building blocks carbon or nitrogen are growth-limiting and are diverted from cellular biomass production. We confirm this result experimentally with a continuous-culture approach. We show that pyoverdine non-producers (cheaters) enjoy a large fitness advantage in co-culture with producers (cooperators) and spread to high frequency when limited by carbon, but not when limited by phosphorus. The principle of nutrient-dependent fitness costs has implications for the stability of cooperation in pathogenic and non-pathogenic environments, in biotechnological applications, and beyond the microbial realm. Cooperative behaviour among individuals provides a collective benefit, but is considered costly. Using Pseudomonas aeruginosa as a model system, the authors show that secretion of the siderophore pyoverdine only incurs a fitness cost and favours cheating when its building blocks carbon or nitrogen are growth-limiting.