Predatory slime mould freezes prey in large groups

This post is part of a celebration of the 2-year anniversary of open-access journal PLoS ONE.

Gathering in large numbers is usually a good way of protection yourself against predators, and it’s no surprise that mass defence is a common strategy in the natural world. But it doesn’t always work. There is one hunter that has found a way to use group defence to its advantage. It allows its prey to gather in large numbers and then freezes them in place with a chemical weapon, providing it with a bountiful banquet to eat at its leisure. It’s called Dictyostelium caveatum.

D.caveatum is a member of the dictyostelids, a group that also goes by the names of “slime moulds” or “social amoebae”. It consists of a single cell and its rather unassuming amoeba-like appearance hides the fact that it is a predator par excellence. Lacking fangs, claws or any of the weapons of multi-celled creatures, it nonetheless has highly effective ways of killing its prey – other very closely related social amoebae.

The majority of dictyostelids, such as D.discoideum, are some of nature’s most vivid examples of cooperation. They live most of their lives as single cells that eat bacteria, but a lack of food drives them to seek out company. Like shattered pieces of a T-1000, single cells move towards each other and stick together to form clumps (left image). These clusters elongate to become multi-celled “slugs” (middle), which in turn reach for the sky and transform into “fruiting bodies” (right) – a long stalk topped by a ball of spores. When food is available again, the spores are released and become new amoebae, starting the cycle all over again. The cells that make up the stalk are left to die, sacrificing themselves for the future of their peers.

It’s a lovely story, but add D.caveatum into the mix and you get a very different ending. If a group of 10,000 D.discoideum cells is invaded by even a single D.caveatum one, they are doomed. The lone invader eventually eats the other species, using their cells as fuel to produce its own fruiting bodies. After 48 hours, only D.caveatum remains. This extraordinary behaviour was discovered about two decades ago by one David Waddell but only last year, Clement Nizak from Rockefeller University managed to observe it for the first time under the microscope and work out how it happens.

(Watch D.caveatum (the red arrows) devour D.discoideum (the green arrows).)

Nizak loaded cells of different social amoebae with fluorescent chemicals, so that he could track their movements under a microscope. His images revealed that D.caveatum, sporting a green glow, are surprisingly active and mobile. When they come across amoebae of D.discoideum (looking fetching in fluorescent red), they send out extensions called pseudopods that surround the prey within seconds. Shortly after, the engulfed victim is broken down. Its only hope of survival is in being large enough that the predator can’t completely surround it.

D.caveatum can also eat other social amoebae after they’ve started to gather into groups as Nizak showed by cutting one of these in half and using a microscope to identify the predatory cells within. But that doesn’t explain how a single D.caveatum can consume a group of tens of thousands of other amoebae, before it can form a fruiting body. It simply shouldn’t have enough time.

Nizak found that D.caveatum gets around its limited time frame by freezing the development of its prey species. When amoebae clump together, they form a distinct mound that tips over to form the front end of the slug. But even small concentrations of D.caveatum cells can prevent the mound from forming and without it, the prey are stuck in the cluster stage and slowly overwhelmed.

D.caveatum manipulates other social amoebae using a chemical that the it constantly secretes. In a wonderfully elegant experiment, Nizak separated D.caveatum and D.discoideum with a  permeable filter that prevented the two species from interacting but would allow molecules to pass from one to the other. On its own, D.discoideum wasn’t affected by the filter but in the presence of D.caveatum (either alone or in a mixture) its development was completely frozen, even without any direct cell-to-cell contact.

Nizak used dialysis to isolate the secretions from D.caveatum and found that these alone could halt D.discoideum‘s life cycle, although for a shorter time than when actual predatory cells were around. The precise identify of the chemical in question is still a mystery, but one thing’s for certain – it doesn’t kill the prey outright and its effects are reversible. If it’s removed, the majority of D.discoideum clumps soon resume their life cycle and produce fruiting bodies. But in natural situations, they wouldn’t get the chance with D.caveatum cells still around to pump out more inhibitors.

This ability to freeze the development of other social amoebae is all the more remarkable for the sheer number of species that are affected. Of the hundred or so species of social amoeba so far discovered, D.caveatum is the only one that has evolved to exploit and prey upon its own kind and indeed, it develops more quickly when it’s fed with other social amoebae than on the group’s traditional diet of bacteria. Nor is it fussy about its choice of prey. Nizak found that they will gorge themselves on at least six different types of distantly related social amoebae, and even one species that isn’t a dictyostelid. Whether it uses different chemicals for each species is a mystery for now.

It only draws the line at cannibalism – if it bumps into cells of its own kind, they go their separate ways. Indeed, D.caveatum is immune to its own chemical weapon, although how it gets away with it is unclear. For the moment, Nizak suggests that D.caveatum may have evolved the ability to prey upon other dictyostelids by losing or modifying the genetic pathways that normally prevent social amoebae from eating each other. In the future, it may be possible to test this idea by studying genetic changes in a mutant cannibal strain of D.caveatum (also discovered by David Waddell), which doesn’t avoid eating other cells of the same species.

(D.caveatum cells meet but don’t eat one another)

For the moment, what we know of D.caveatum shows it to be a surprisingly sophisticated predator that uses finely tailored chemicals to alter the behaviour of its prey. There are plenty of other similar examples in the natural world. Just last year, I blogged about the emerald cockroach wasp which uses cockroaches as living larders for their young. It injects them with a venom that specifically reduces their motivation to walk, but not their general motor skills. The upshot is that the wasp can grab a stung cockroach by its antennae and walk it around like a dog on a leash.

Reference: Clement Nizak, Robert J. Fitzhenry, Richard H. Kessin (2007). Exploitation of Other Social Amoebae by Dictyostelium caveatum PLoS ONE, 2 (2) DOI: 10.1371/journal.pone.0000212

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