CORVALLIS, Ore. - If you've got plenty of burgers and beers on hand and your own stomach is full, an uninvited guest at your neighborhood barbecue won't put much strain on you.

But if you're hungry and food and drink supplies are running low when the moocher shows up, it's a different story.

New research at Oregon State University indicates bacteria know just how you feel.

Microbes that produce important secretions for use in a community suffer a blow to their own fitness for supplying the non-producing "cheater" bacteria - but only when production requires the same nutrients that would otherwise go into growth and biomass.

Findings were published today in Nature Communications.

Bacteria are important organisms for evolutionary biology research because their fast growth allows scientists to study evolution in real time in the lab. The common, rod-shaped bacteria in the study, Pseudomonas aeruginosa, can lead to infections in humans, and cheater strains are often found among the infection-causing organisms.

"The big picture of this research is a better understanding of how cooperation works and how cooperation evolved," said corresponding author Martin Schuster. "We can use microbes to study social evolution. Essentially every environment is nutrient limited in some way, and our study allows us to make predictions about what types of environments are conducive to cooperation or cheating."

The study by Schuster and 2017 Ph.D. graduate Joe Sexton involved P. aeruginosa and a peptide siderophore it secretes, pyoverdine, or PVD.

P. aeruginosa uses PVD to scavenge iron, an essential and hard-to-get nutrient; the cheaters don't produce PVD but have a receptor to collect the iron the siderophore binds with.

"The secretions benefit everyone, and cheating bacteria don't participate in the production," said Schuster, associate professor in OSU's Department of Microbiology in the colleges of Science and Agricultural Sciences. "In general, cooperation is considered costly; therefore, cheaters can exploit the process by saving on the costs of cooperation."

Building on earlier studies that showed cooperative behavior in P. aeruginosa can be exploited by mutant cheaters, this research demonstrates that the costs of bacterial cooperation are conditional.

"It's all contextual and depends on the environment, the available nutrients, the bacterial diet," Schuster said. "Sometimes cooperation is very costly, other times not at all. And if cooperation isn't costly, it means that cheating doesn't provide an advantage."

In the case of PVD secretion, there's a fitness cost involved for P. aeruginosa when carbon or nitrogen are in limited supply; those are building blocks for PVD and also necessary for producing cellular biomass.

But shortages of other nutrients - iron, phosphorus and sulfur - don't result in a fitness cost; thus, the cheaters don't gain an edge in those scenarios.

"Before, fitness cost was thought to be proportional to how much siderophore was being made," Sexton said. "We showed that under different nutrient conditions the bacteria were still making the same amount, but the fitness costs varied dramatically."

The researchers experimentally verified their modeling predictions with a chemostat format, an open system in which fresh nutrients flow in at the same rate spent growth medium flows out; cell density and growth rate are kept constant. In this system, the fitness costs of PVD production were apparent as growth differences between cooperators and cheaters in a mixed culture.

"In addition to fundamental questions about the evolution of cooperation, our work is also relevant to natural populations," Sexton said. "There are siderophore-negative strains in the soil and the ocean and in human infections. Where did they come from? Did they evolve as cheaters, or for some other reason? Our work provides a new piece of the puzzle to consider in real-world contexts."

The National Science Foundation and the Alexander von Humboldt Fellowship for Experienced Researchers supported this research.

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Steve Lundeberg, 541-737-4039

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