Dicty spore capsules on their stalks. Credit: Scott Solomon
Dicty spore capsules on their stalks. Credit: Scott Solomon

The Bacteria That Turn Amoebas Into Farmers

Most people think of bacteria as germs, signs of filth, or unwanted bringers of disease. Slowly, that view is changing. It is now abundantly clear that the bacteria that live on the bodies of other creatures help their hosts by digesting food, providing nutrients, protecting against disease, detoxifying poisons, slaughtering prey, and even creating light. The list of surprising abilities is extensive, and just when you think it might run out, someone comes along and shows that bacteria can turn amoebas into farmers.

The amoeba in question is Dictyostelium discoideum, or Dicty to its friends. It mostly lives as a single cell that engulfs and eats bacteria. But when food is scarce, these solitary cells congregate and merge into a many-celled slug. The slug oozes about until it finds a good spot, whereupon it stretches skywards to form a ball at the end of a stalk. The ball is full of spores, which eventually blow off, seeding some far-off (and hopefully more bountiful) area with new amoebas.

Back in 2011, Debra Brock and her colleagues showed that Dicty sometimes packs several species of edible bacteria in its slugs and spores. When the spores land somewhere new, their bacteria cargo multiples, creating a ready supply of food. Brock described these bacteria-carrying amoebas as “farmers”. They lugged their ‘crops’ around and ‘planted’ them to provide bountiful meals in unfamiliar terrain.

The metaphor is apt but, like all of them, comes with baggage. It suggests that the amoebas are actively in control of their passive bacterial crops—and that’s not entirely true. The same team of scientists, led by Joan Strassmann and David Queller at the Washington University in St Louis, have now found that some bacteria can turn Dicty into farmers in the first place!

The team already knew that the farming strains of Dicty carry diverse communities of bacteria. These include species like Klebsiella which serve as food, and other inedible microbes that just go along for the ride. And though these inedible bacteria varied from one amoeba to the next, postdoc Suzanne DiSalvo found that one species—Burkholderia—was universal. It turned up in all the farmers.

Burkholderia has a penchant for symbiosis—that is, for forming associations with other organisms. There are strains that cause opportunistic infections in people, that allow bugs to instantly resist insecticides, that donate antibiotic-producing genes to animals, and that provide various benefits to plants. What do the ones in Dicty do?

DiSalvo eventually figured out that they are largely (maybe even entirely) responsible for Dicty’s farming lifestyle. She could turn non-farming amoebas into bacteria-carrying farmers by giving them the right Burkholderia strains. And she could permanently “cure” these farmers of their ability to transport bacteria by treating them with antibiotics. “This was very exciting and amazing,” says Strassmann.

It’s not clear how Burkholderia does this, but the fact that the amoebas can’t eat it is probably important. “I think the Burkholderia are infecting Dicty and disrupting some process whereby it digests its bacterial food,” DiSalvo speculates. Inadvertently, this also means that Dicty can now carry around other bacteria that it would normally digest. That’s the core of its farming behaviour: the ability to harbour microbes without harming them, rather than immediately destroying them for food. Burkholderia, by selfishly protecting itself from digestion, also gives the amoebas the basis of their agriculture.

This transformation comes with costs. Dicty faces obvious disadvantages if it can’t efficiently digest its food. Indeed, DiSalvo found that if there’s a lot of food around, the farmers produce fewer spores than non-farmers, and are less successful. But when food is scarce, the balance of benefits and costs flips. Now, the farmers, which can carry bacteria to new pastures, do better than their non-farming peers.

These results illustrate one of the most important aspects of symbiosis, and one that is often overlooked: it is contextual. The same microbe can be harmful to its host in one setting but beneficial in another. In one context, it’s a parasite; in another, it’s a mutualist. “This work highlights the fragility of incipient symbioses,” says John McCutcheon from the University of Montana, who reviewed the paper. “It shows how pathogenic and mutualistic outcomes can teeter along a rather thin edge, tipping one way or the other in a manner dependent on complex environmental factors.”

It’s also a great example of how bacteria can directly influence the behaviour of more complex hosts, McCutcheon adds. While many scientists are studying the microbes of the human body, and their effects on our health and behaviour, these studies are almost entirely correlative. That is, they simply compare the microbial communities in different groups of people. But with simple organisms, like Dicty, Strassmann’s team isn’t so limited. They can do experiments.

The team are now trying to slowly knocking out Burkholderia’s genes to identify those that help it to colonise Dicty. They’re studying the cycle of infection under the microscope. And they’re looking at the chemicals that the two partners use to communicate with each other. “It’s a blast,” Strassmann adds.

Reference: DiSalvo, Haselkorn, Bashir, Jimenez, Brock, Queller & Strassmann. 2015. Burkholderia bacteria infectiously induce the proto-farming symbiosis of Dictyostelium amoebae and  food bacteria. PNAS http://dx.doi.org/10.1073/pnas.1511878112

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