Elysia crispata, the frilly green lettuce sea slug, has a remarkable adaptation: It can photosynthesize. The slugs use their scraping tongues to pierce algal cells, then suck up the contents like a smoothie. Ingested chloroplasts are absorbed into the slug's gut-lining cells, where they photosynthesize, making glucose for days to months. A recent study in Cell sheds new light on how slugs accomplish this feat: by packaging ingested chloroplasts into their own membrane-bound compartments inside the slug gut cells.
"Part of how the slugs are able to steal organelles," says lead author Corey Allard, "is that they put them in yet another organelle, a storage organelle, that seems to let the slug control how the cargo gets used." Allard, a cell physiologist at Harvard Medical School in Boston, and his coauthors named this new organelle the "kleptosome." It may offer some insight into the evolution of symbiosis.
Marine biologists have studied photosynthetic sea slugs since at least the 1970s. But how the slugs hijack chloroplasts remained unclear. Searching for answers, Allard looked to the cell biology and biophysics of organelle theft.
He first purified chloroplasts out of slugs, extracting chloroplast proteins and running them through a mass spectrometer to identify them. Oddly, most of the proteins distilled from the chloroplasts weren't algal. "What we got back, instead, was a laundry list of mostly slug proteins," he says. It turns out that some of the slug proteins identified were associated with phagocytosis and endocytosis, hinting that the slug cell had engulfed the chloroplasts in another membrane-bound compartment, the kleptosome.
But was the kleptosome actually helping the slug steal chloroplasts or photosynthesize? To find out, Allard and his team disabled the kleptosome membrane using a drug to stop ions from crossing one type of membrane ion channel. With the ion channel inhibited, cellular oxygen production from photosynthesis significantly declined. Allard concluded that the kleptosome must be mediating photosynthesis, though questions remain about the exact mechanism.
The team also noticed that when slugs hadn't eaten for weeks to months, they changed color from green to orange, "like leaves in fall," Allard says. It turns out their chloroplasts had broken down. Starving slugs had degraded chloroplasts and kleptosome membranes under the microscope. Allard observed an increase in digestive lysosomes in starving slug cells, and hypothesizes that the membrane fuses with lysosomes to digest the chloroplasts as a last-ditch food source.
"It's a clever and rigorous piece of work.," says marine biologist Sónia Cruz at the University of Aveiro, in Portugal. Cruz, who specializes in algae and symbiosis, lauds the paper for not only identifying the kleptosome organelle, but also showing that the membrane has active ion transport that affects photosynthesis. In addition, the work reframes slug photosynthesis as an active process of integrating chloroplasts into organelles, rather than a more passive process of simply stashing chloroplasts in the cell's cytoplasm.
Some functions of the chloroplasts remain an open question, however there's not much of nutritive value in the chloroplast (it's mostly membranes), and most slug cells don't contain chloroplasts, so it seems unlikely they'd be a nutrition source during starvation, notes Sidney Pierce, a retired molecular physiologist at the University of South Florida, who's published widely on sea slug photosynthesis. "No one knows the biochemical basis of how [chloroplasts and] photosynthesis is maintained in the animal, outside the algae," he says. Digestion in mollusks like the sea slug happens inside digestive cells lining the gut (which Pierce would expect to contain lysosomes), but finding degraded chloroplasts doesn't necessarily mean they have nutritional value.
Allard acknowledges that starving slugs may not use the chloroplasts as a fuel source. "To me," he says, "the idea they're breaking them down for nutrients seems plausible and makes the most sense, but certainly one could imagine alternatives." Lysosomes break things down into building blocks to use them for nutrition. But it is possible, he notes, that when slugs are very stressed their chloroplasts release additional stressors, such as reactive oxygen. The slug could attack the chloroplasts to reduce these other stressors.
In any case, finding a new organelle is not only a step toward understanding the sea slugs. The work also could actually offer clues about the evolution of symbiosis, hinting at the cellular processes that let one organism engulf and maintain another. Learning how these events happen at a molecular level, Allard says, may reveal some general biochemical mechanisms that enable the evolution of symbiosis.
About two dozen species of sea slugs hold onto chloroplasts. Some can maintain them for a year; others for only a few hours or days. Looking ahead, Allard is now repeating these experiments in several more species, to "get a sense of what's different between them," and which molecules or cellular processes are unique to slugs that maintain their chloroplasts long-term.
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