The Helpful Pacifism of Bacterial Cheaters

cheatingHave you ever cheated on a test by glancing over at someone else’s work? Or relied on a fellow student to carry the load on a group project while you coast along with minimal effort? While few will admit to these forms of cheating, they have long been fixtures of the classroom. However, a lazy individual benefiting from the hard work of a colleague is not a trick exclusive to humans. In a recent study of bacterial infections in plants, the laboratory of evolutionary biologist Joy Bergelson demonstrated that these unsavory practices can also be found in pathogens – and that may be a good thing for us.

In the bacterial world, the goal is survival. What we perceive as an infection is merely colonization for the bacterial population, who are establishing a new home where they can happily feed off the host’s nutrients and reproduce. Bacteria build and release virulence factors to achieve this settlement and evade immune system defenses. But because these factors spread out, benefiting an individual bacterium’s neighbors as well as itself, a sneaky bacterium can get by without producing its own virulence factors. In laboratory dish experiments, scientists observed that bacteria engineered without the ability to release factors can still thrive so long as they are paired with normal, pathogenic partners.

Though scientists described this “cooperator-cheater model” in the artificial environment of the dish, nobody had yet observed it in a natural setting. For a study published in September by the journal Ecology Letters, a team led by postdoctoral fellow Luke Barrett discovered the model in action within the cells of the popular genetic model plant Arabidopsis thaliana.

“We’re showing that cheating actually happens in nature, and that the cheaters persist,” Bergelson said. “You can make cheaters that do well in the lab, and you can show that these systems may be stable in theory, but to show that it is actually happening in nature is novel.”

Recently, researchers discovered that Arabidopsis carried two strains of the bacteria Pseudomonas syringae, a common plant pathogen. While one strain had all the normal pathogenic activity, another was a kind of bacterial pacifist, with a broken system for secreting virulence factors. Surprisingly, these two strains appear with almost equal frequency in Arabidopsis, suggesting that the non-pathogenic strains are far more successful in nature than previously thought.

To test the nature of this relationship, researchers took the two natural strains and experimentally infected plants with only one or the other. When grown alone, the “cheater” strain was not nearly as successful without its more aggressive partner around to unwittingly “donate” virulence factors. Additional modeling suggested that the more aggressive the virulent strain, the more likely it was that cheaters would be found nearby eager to exploit the hard work of their pathogenic peers. The cheater strains are also harder for the host immune system to spot, since the machinery that produces and releases virulence factors is a frequent target of those defenses.

“When you go into the field, it’s kind of a curiosity: why would non-pathogenic cheaters be almost as common as pathogens inside the host?” Bergelson said. “It turns out that the cheaters can do really well as long as they’re with the pathogenic variety, and they don’t pay the price of having to actually make a secretion system or effectors. They also don’t run any risk of being recognized because it is the presence of secreted effectors that causes the recognition events in the first place. So, these non-pathogens have some good things going for them.”

Despite this evidence for a cooperator-cheater model in nature, a mystery remained. If cheaters depend upon more aggressive partners to infect a host, one would expect them to be far more vulnerable to extinction since they cannot fend for themselves. But that speculation only takes half of the bacterial world into account, by focusing only on its time infecting a host. Before a bacterium reaches the promised land of infection, it must survive in the external environment — which in the case of P. syringae, means water and soil.

In this environment, the aggressive strains are at a disadvantage, because of the biologically expensive weaponry they sport. The research team discovered that cheater strains, which don’t waste valuable energy on building the cellular machinery to infect a host, showed higher fitness outside of the plant. Thus, the balance between success inside and outside the plant kept the cheater and cooperator strains of P. syringae in a kind of equilibrium.

“The benefit that cheaters get [from not having the secretion system] compensates for their failure to infect hosts without the cooperator being present,” Bergelson said. “It’s sufficient to maintain them in the system.”

In the end, the cheating ways of bacteria may be good news for humans. Many pathogen models have argued that bacteria will grow increasingly dangerous, as more and more aggressive strains evolve driven by selective pressures such as antibiotic treatment. But if the total population of an infectious pathogen contains both aggressive cooperator strains and toothless cheater strains, the net virulence of a given infection should be constrained, preventing a runaway arms race with grave health consequences.

“The fact that cheaters have evolved from non-cheaters and now contribute to the pool of isolates that will infect the host means that the overall system has evolved to be less aggressive, because it has come to contain a combination of aggressive strains and non-aggressive strains,” Bergelson said. “That idea counters what had been the prevailing view, that virulence is only going to increase in this escalating process. Here, it seems to be just the opposite.”

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Barrett, L., Bell, T., Dwyer, G., & Bergelson, J. (2011). Cheating, trade-offs and the evolution of aggressiveness in a natural pathogen population Ecology Letters, 14 (11), 1149-1157 DOI: 10.1111/j.1461-0248.2011.01687.x

About Rob Mitchum (518 Articles)
Rob Mitchum is communications manager at the Computation Institute, a joint initiative between The University of Chicago and Argonne National Laboratory.
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