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Solar-Powered Slugs Are Not Solar-Powered

Good science is about resisting the pull of easy conclusions. It’s about testing stories that seem like they should be right to see if they actually are right.

This is no easy task. Consider the case of the “solar-powered” slugs.

There are four species of green sea slugs that supposedly can photosynthesise, just like plants. That is, they can make their own food by harnessing the power of sunlight. This skill is almost unheard of for an animal, but the slugs pull it off through an act of thievery. They steal chloroplasts—the little solar panels where photosynthesis takes place—from the algae that they eat, and store them in their bodies for several months.

The chloroplasts give them their beautiful green colour, and apparently allow them photosynthesise. You can keep them in a lab for several months without any food, and they’ll survive as long as you shine a lamp upon them.

It seemed obvious that the chloroplasts were responsible. Photosynthesis means sugar, sugar means food, food means survival. The chloroplasts provided the slugs with internal nourishment, just as they do in plants. Many scientists and journalists (including myself) started describing the slugs as “leaves that crawl” or “solar-powered” animals.

At first, Sven Gould from Heinrich-Heine University in Dusseldorf was part of this bandwagon. But the more he looked into the story, the more he realised that something wasn’t right.

He started reading papers that go back 40 years, and realised that when the slugs are starved, they grow smaller and paler with time, even when they’re exposed to light. Weirder still, some starved slugs survived just fine in the dark, while others that were kept in the light would die. Why?

To find out, graduate student Gregor Christa worked with two green sea slugs—Elysia timida from the Mediterranean and Plakobranchus ocellatus from the Philippines. He showed that when exposed to light, they convert carbon dioxide in the air into sugars—the essence of photosynthesis.

Next, Christa stopped the starving slugs from photosynthesising, either by keeping them in the dark for three months or by using chemicals. To everyone’s surprise, they survived just as well as animals that were kept in the light, and they lost just as much weight. “It was a very easy experiment,” says Gould. “You put them in the dark, take them out after four weeks and they’re all happy. That was quite a shock.”

The team concluded that the green slugs are not solar-powered. Even though they effectively have solar cells in their bodies, they don’t need to photosynthesise to survive.

“We know that we were hitting a wasp’s nest,” says Gould. “It’s like covering a beautiful piece of sushi in wasabi—it becomes hard to digest and swallow.”

Elysia timida. Credit: Parent Gery
Elysia timida. Credit: Parent Gery

He thinks that the chloroplasts are acting as food reserves—less like a plant’s leaf and more like a camel’s hump. They are loaded with fats, proteins and nucleic acids like DNA. The slugs could subsist on them when they run out of algae to graze upon. That would explain why they can endure a bout of starvation in the dark, and also why they shrink and get paler over time. “It’s pure speculation and a working hypothesis,” says Gould.

“The notion of the slugs storing chloroplasts as some sort of a food hoard seems a bit gratuitous,” says Sidney Pierce from the University of South Florida. “The plastids are only in a relatively few cells and would not seem to be much of an energy source on their own.” He adds that what is true for the species that Gould studied may not apply to all green slugs. “If their results are correct, they are very likely just species differences and the authors may be over-generalizing.”

Gould admits that other slugs like E.chlorotica—the species that the Americans have focused on—may depend on photosynthesis more strongly… but he doubts it. In winter, E.chlorotica digs itself into the mud and survives for months. “If it’s in the mud, how does it get enough light?” asks Gould. “We need to check this. Maybe we’ll be surprised and they really do die, but I doubt it.”

And there’s yet another mystery about the slugs: how do they photosynthesise at all? Chloroplasts need between 1,000 and 3,500 proteins to carry out photosynthesis. They can make between 60 and 200 because they have their own tiny genomes but for the rest, they depend on the DNA within the nucleus of their host cell. When the slugs steal the chloroplasts from their algae, they leave the nucleus behind. On their own, the chloroplasts simply shouldn’t work.

“That’s the biggest riddle,” says Gould. “Every time we give talks, plant scientists cannot believe that there are chloroplasts that perform for months and months without nuclear genes. That is not possible.”

To explain this paradox, some scientists have suggested that the slugs have also stolen genes from the algae, patching their own genomes to make themselves photosynthesis-compatible. In 2008, Mary Rumpho found evidence of one such photosynthesis gene—pbsO—in the genome of the green slug Elysia chlorotica.

But now, it seems that this result was a false alarm. In 2011, the German team found no evidence that E.timida and P.ocellatus are activating PbsO, or any other algal nuclear genes. Shortly after, Rumpho’s team showed that the same applies to E.chlorotica.

So, the stolen chloroplasts can clearly carry out photosynthesis, but we don’t know how it happens and, in at least two species, we don’t know what it’s for. “It’s an utterly complex and bizarre system,” says Gould. “It’s very difficult to digest.”

“A lot of work that’s been done on the slugs has focused on too many things at once,” he says. “[People have] confused the plastid longevity with slug survival, or gene transfer with plastid longevity. We need to tackle one tiny question after the other.”

PS: One more question: The four green slug species are relatives, but they’ve all evolved their chloroplast-hoarding ways independently. Other sea slugs have a similar trick—they eat jellyfish, steal their stinging cells, and shunt them into their own extremities. During their early evolution, these slugs seem to have gained the ability to pilfer cellular components from their food, and different lineages do it in different ways. Why? No one knows.

More on animal photosynthesis:

7 thoughts on “Solar-Powered Slugs Are Not Solar-Powered

  1. I’d just like to comment on a few things here. We did not directly conclude they are not solar-powered, but could demonstrate that they do not need light as a prerequisite to survive starvation. That is an important difference. Like LGT (lateral gene transfer) does not explain kleptoplast longevity in slugs, photosynthesis alone does not explain slug survival during starvation. It’s just all not as easy, as we might want it to be.

    Dr. Pierce’s comments puzzle me bit. Not as much as his work on LGT in slugs, but still a bit. Fact is, the slugs are so full with plastids that they’re green (look at for instance the image associated with this article or the Nature news piece: http://www.nature.com/news/solar-powered-sea-slugs-can-survive-in-the-dark-1.14197). Also, the plastids are very much an energy source of their own. They’re packed with all the good stuff: proteins, lipids, starch, nucleic acids and trace elements. In any case, yes, the observations are uncomfortable, but that’s the data that work by others confirms (e.g. Klochkova et al. 2013).

    Next big thing will be to explain kleptoplast longevity. That remains the biggest brainteaser regarding these slugs.

  2. Perhaps the slugs use both?
    Photosynthesis regardless of mechanism is something they do, correct?
    If so perhaps the photosynthesis is used to supplement an otherwise impoverished portion of their diet and that is the reason they can survive in the dark, or mud.
    Essentially what I’m trying to get at is perhaps if they are photosynthesizing it isn’t essential for survival but makes their diet more rounded, akin to a bear not NEEDING berries but benefiting from them.

    1. @Riven: You’re absolutely right, couldn’t agree more, and that is pretty much what we’re saying: not directly essential for survival, but maybe some hidden benefit we yet need to discover.

    1. Yep, it seemed so obvious and yet the last couple of years have shown as that not everything in the slugs is like we thought it is. Also, they might be “solar-powered“ for another reason, but not for core-carbon metabolisms, or better to survive starvation like we all thought. Actually not everyone, some before us (labs from Asia and Europe) have questioned the importance of photosynthesis for the slugs, but did not test it so directly.

      The lateral gene transfer (LGT) hypothesis in slugs (the psbO gene, a PNAS story) also seemed convincing, but has proven wrong. Also the careful check by the original authors of the LGT story themselves (Rumpho et al.) can no longer find evidence for it. We’ll see what the future holds.

  3. Very interesting findings. I am not familiar with the literature, but it seems that calling these sea slugs “solar-powered” was a stretch to begin with. Even the energy provided by algal symbionts (e.g. zooxanthellae) to cnidarian hosts (e.g. corals, sea anemones) has been called “junk food” by certain authors, since most of the carbon translocated to the host is used in respiration rather than growth. Obviously the slug-chloroplast relationship is different, but maybe parallels can be drawn.

    As for the hypothesis that chloroplasts serve as a food reserve, it would be interesting to run the experiment with more slugs (replicates) and observe if the slugs with chloroplasts lose weight slower than those that have been stripped of their chloroplasts.

  4. it’s interesting knowing that there’re creatures out there having such uniqeness within their system. This mysteries yet to unfold, but i’m looking forward to read some new articles related to this topic.

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