The social amoeba Dictyostelium discoideum is scientists’ go-to model for studying multicellularity, chemical signaling, and many other biological phenomena. Found in soil, the single-celled “dicty” crawls around, eating bacteria. During starvation, it joins with thousands of other dicty cells to form a so-called slime mold, with the individual cells competing and cheating to form a fruiting body. The fruiting body then forms spores, which re-enter the life cycle when they wind up in places that have more edible bacteria.
In 2011, Joan Strassmann, David Queller, and their team (then at Rice University in Houston, Texas) discovered that about one-third of dicty colonies act like primitive farmers by carrying, seeding, and harvesting several strains of bacteria (1).
Intriguingly, the farmer dicty only consumes about half of the bacteria it plants. But the purpose of the inedible bacteria remained unclear.
In a new study published July in Proceedings of the National Academy of Sciences, Strassmann and Queller, now at Washington University in St. Louis, Jon Clardy at Harvard Medical School in Boston, and their teams have demonstrated that the non-food bacteria help preserve the dicty. Interestingly, a single genetic mutation distinguishes this bacterial strain from one of dicty’s meals (2).
Examples of complex cooperative relationships underlying primitive farming can be found in other kingdoms. For instance, some ants carry and farm a fungus that relies on the ants to survive, but the ants also carry bacteria that release small molecules for protection.
“Given the way the [these] other systems worked, it seemed clear to me that [the nonfood bacteria] were probably making some sort of chemical defense,” explains Clardy.
To find out, the team analyzed metabolites produced by food and non-food bacteria—in this case, two different strains of the gram-negative bacterium Pseudomonas fluorescens. It turns out that the inedible strain, PfA, produces both pyrrolnitrin and a previously unknown molecule called chromene.
Pyrrolnitrin was toxic to non-farmer dicty but not to farmer dicty, showing that farmer dicty has acquired a resistance to the toxin. In addition, chromene boosted spore production in the farmer dicty but decreased spore production in the non-farmer strain.
Comparing the sequence of gacA—a gene encoding metabolites produced from the bacteria—from PfA to that of the food strain, PfB, the group identified a single point mutation in gacA that resulted in a shortened protein product.
“In many ways, the most interesting part of the paper is how little you had to change to get from one kind of bacteria into another,” says Clardy. “I think it would be worth going back into the environment and seeing if we can find, away from the amoeba, those two kinds of bacteria related by the same mutation.”
The two strains of bacteria are very closely related, suggesting that one strain diverged evolutionarily from another. “The question then is, where did that happen?” says Clardy.
One possibility is that dicty picked up the PfA and carried it for protection, and then the PfA evolved into a food source. Another possibility is that the dicty picked up both strains of bacteria at the same time, and then began to evolve to become more tolerant of the PfA because it produces metabolites that kill off fungi and other pathogens.
Farmer dicty also carries other kinds of bacteria. “There are many other stories to be learned from the different kinds of bacteria,” says Clardy. “We might find other pairs that have the same sort of relationships.”
Overall, “this is a very interesting example and further indication of the importance of these small molecules in mediating species interactions,” notes Cameron Currie, professor of bacteriology at the University of Wisconsin-Madison, who was not involved with the study but has collaborated with Clardy’s group in the past.
“The findings provide further indication that these complex [multi-partite] interactions [across kingdoms] are likely more the norm than the exception,” adds Currie.
1. Brock, D.A., Douglas, T.E., Queller, D.C., Strassmann, J.E. 2011. Nature. Primitive agriculture in a social amoeba. 469(7330): 393-6.
2. Stallforth, P., Brock, D.A., Cantley, A.M., Tian, X., Queller, D.C., Strassmann J.E., Clardy, J. 2013. A bacterial symbiont is converted from an inedible producer of beneficial molecules into food by a single mutation in the gacA gene. Proc Natl Acad Sci USA. Jul 29. [Epub ahead of print]