Many bacteria have an incredible ability to swarm cooperatively over surfaces. But swarming phenotypes can be quite different even between strains of the same species. What drives this diversity? We compared the metabolomes of 29 clinical Pseudomonas aeruginosa isolates with a range of swarming phenotypes. We identified that isolates incapable of secreting rhamnolipids—a surfactant needed for swarming—had perturbed tricarboxylic acid (TCA) cycle and amino acid pathways and grew exponentially slower in glycerol minimal medium. Analysis of the metabolome signatures and simulations using a genome-scale model led to a mechanism which joins these observations: Strains subject to higher oxidative stress levels grow slower and shut down rhamnolipids secretion, a carbon overflow mechanism possibly to direct carbon resources towards costly stress response pathways to maintain cell viability. In vitro experiments confirmed that rhamnolipid non-producers deal worse with oxidative stress, linking intracellular redox homeostasis—a individual-level trait—to swarming—a population-level behavior. This mechanism helps explain the metabolic constraints on bacteria when secreting byproducts to interact with others—competitively and cooperatively—in microbial communities. Significance Swarming motility has been associated with virulence of many human bacterial pathogens. The pathogen Pseudomonas aeruginosa swarms by cooperatively secreting surfactants called rhamnolipids to lubricate surfaces. To understand why some P. aeruginosa strains swarm and others do not, we combined metabolomics, computational modeling and in vitro experiments to study the different swarming behaviors of 29 isolates of Pseudomonas aeruginosa obtained from infected patients. We found that strains can only produce rhamnolipids if they can maintain redox homeostasis. We propose that single cells must have low internal redox stress levels before they can produce rhamnolipids, which work as an overflow of carbon metabolism into a cooperative secretion that brings a fitness benefit to the entire swarming population. This mechanism links single-cell physiology and a population-level cooperative behavior key to the fitness and virulence of P. aeruginosa , a major source of hospital acquired infections. ![Figure]</img> Synopsis This study combined metabolomics, computational modeling and experiments to explain the swarming diversity in Pseudomonas aeruginosa , yielding new insights on the genetic and metabolic controls of bacterial swarming behavior ### Competing Interest Statement The authors have declared no competing interest. : pending:yes
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