How Sea Slugs Steal Chloroplasts: The Strange Biology of Kleptoplasty

In the warm shallow waters of the western Atlantic and Caribbean, a small green sea slug called Elysia chlorotica lives a life that breaks most of the rules of animal biology. It looks like a curling leaf, about three centimeters long, with two delicate horn-like appendages on its head. It spends most of its day basking in the sun. It does not eat for most of its life, surviving on photosynthesis. The chloroplasts that produce that photosynthesis are not its own. It steals them from algae, and once it has enough, it does not need food again.

The phenomenon is called kleptoplasty, from the Greek for "stolen plastids," and it is one of the most surprising integrations of separate kingdoms of life that has ever been described. The mechanism keeps producing surprises because the standard story of how organelles work, learned in introductory biology, cannot fully account for what these animals do.

The basic biology

The slug eats Vaucheria litorea, a filamentous yellow-green alga that grows in tidal marshes. Like all algae, Vaucheria's photosynthesis happens in chloroplasts: small bean-shaped organelles, descendants of an ancient cyanobacterial endosymbiont, that contain the chlorophyll, the photosystems, and most of the machinery for converting light and carbon dioxide into sugar. The slug pierces the alga's cell wall with a row of small teeth called a radula, sucks out the cytoplasm, and digests it. Most of the cell contents are broken down for nutrients in the usual way.

The chloroplasts are different. Rather than being digested, they are routed to specialized cells in the slug's gut lining, where they are taken in (without being broken down) and held in cellular vacuoles. The cells are arranged in a branching pattern that extends throughout the slug's body, giving the slug its leaf-like green color. Inside those vacuoles, the chloroplasts continue to photosynthesize, exactly as they did inside the algal cell, for as long as the slug lives. A juvenile slug fed enough algae to fill its body with chloroplasts can survive without further feeding for up to ten months, on photosynthesis alone.

The slug is, in a fairly literal sense, partly a plant. It is the most extreme case of kleptoplasty known, and it is the only animal known to live a substantial portion of its life as a functional photosynthetic organism.

The mystery: chloroplasts should not work that long

Here is the biology problem that makes kleptoplasty surprising. Chloroplasts, like mitochondria, are descendants of free-living bacteria that became permanent endosymbionts of eukaryotic cells about 1.5 billion years ago. Over that time, most of the genes that once lived in the chloroplast's own genome have been transferred to the host cell's nuclear genome. The chloroplast keeps only about 100 genes of its original few thousand; the other proteins it needs to function are encoded by the host's nuclear DNA, manufactured in the host's cytoplasm, and imported into the chloroplast through transport machinery in the chloroplast's outer membrane.

The chloroplast cannot function for very long without this constant import. Chloroplast proteins turn over (degrade and need replacement) on timescales of days to weeks. Without the host's nuclear machinery producing replacement parts, a chloroplast should run down within a few weeks at most.

The Vaucheria alga that Elysia eats has its own nucleus, of course, and the nucleus is digested when the slug eats the alga. The slug's own nucleus has no genes for chloroplast maintenance: it is an animal nucleus, with no plant ancestry. By the standard biology, the slug's stolen chloroplasts should stop working within a few weeks.

But they do not. They keep working for months. The slug survives the whole non-feeding portion of its life on them. Something is keeping those chloroplasts running, and what it is has been the subject of an ongoing scientific argument.

The horizontal gene transfer hypothesis (and its problems)

The first proposed answer, in the early 2000s, was that genes had been horizontally transferred from Vaucheria to Elysia over evolutionary time. Mary Rumpho's lab at the University of Maine reported in 2008 that they had found algal genes (specifically, the psbO gene for the manganese-stabilizing protein of photosystem II) in the slug's genome, suggesting that the slug had acquired chloroplast maintenance genes from its algal food and was using them to keep the stolen chloroplasts working.

This finding was reported as a major discovery: the first known case of horizontal gene transfer from one multicellular kingdom to another, with potential implications for evolutionary biology and biotechnology. The story made textbooks within a few years.

The story did not survive replication. In 2013, a paper by Gregor Christa and colleagues in Proceedings of the Royal Society B sequenced the slug's genome and could not find the algal genes that had been reported. In 2014, a paper by Bhattacharya, Pelletreau, and colleagues using deeper sequencing again failed to confirm horizontal gene transfer in Elysia chlorotica. The current consensus in the field is that the original reports were contaminated with algal DNA from gut contents, and that the slug does not, in fact, contain horizontally transferred algal nuclear genes. The chloroplasts are running on something else.

What might actually be going on

The current best guess is some combination of three mechanisms, none of which has been definitively confirmed:

Chloroplast-encoded genes do more than expected. The chloroplast's own small genome includes a few hundred of the genes it needs for photosynthesis, and recent work has revisited the question of whether the chloroplast might be more genetically autonomous than was previously assumed. In Vaucheria specifically, the chloroplast genome retains an unusually large complement of photosynthesis-related genes compared to many other algal lineages. This may be part of why Vaucheria chloroplasts work so well as kleptoplasts: they need less host support to function.

Chloroplast turnover is slower in the dark or low-light environments where the slug typically lives. Chloroplast protein turnover is largely driven by photodamage from intense light. The slug positions itself in moderate light, which reduces photodamage and slows the rate at which chloroplast proteins need replacement.

The slug's cellular environment may provide some non-specific maintenance support. Animal cells have their own protein-quality-control machinery (chaperones, proteases) that may be able to substitute imperfectly for the missing algal nuclear support, keeping chloroplasts working at reduced efficiency rather than failing entirely.

None of these is a complete answer, and the field is still arguing about the relative contributions. The slug remains a working example of a biological phenomenon that does not fit the standard model.

The other kleptoplasts

Elysia chlorotica is the most extreme case, but it is not alone. Several other sacoglossan sea slug species do similar things with different algal sources and with widely varying retention times. Elysia timida from the Mediterranean retains chloroplasts for up to two months. Plakobranchus ocellatus from the Indo-Pacific retains them for several weeks. Elysia clarki from the Caribbean retains them for only a few days, despite eating similar algae.

The variation across species is itself revealing. If horizontal gene transfer were the mechanism, you would expect the species with longest retention to have the most algal genes. Instead, the variation seems to correlate with the source algae (specifically how many photosynthesis genes those algae keep in their chloroplast genome) and with behavior (how much light exposure the slug accepts). This is more consistent with the "chloroplasts run on their own internal capacity" model than with the gene-transfer model.

Several non-slug kleptoplastic organisms are known: some single-celled ciliates, some foraminifera, and some dinoflagellates have all evolved to retain chloroplasts from prey. In these cases, the retention is usually shorter than in Elysia, on the order of days. The shared pattern is that kleptoplasty seems to be relatively common as a short-term phenomenon and rare as a long-term phenomenon, and Elysia chlorotica's several months are the upper end of what has been documented.

What this means

The biology textbook account of organelles as fully-integrated, host-nucleus-dependent endosymbionts is correct in most cases. The chloroplast in a plant or alga cell is part of an integrated system that has been co-evolving for over a billion years, and the chloroplast cannot survive removal from its host. The kleptoplasts show that this integration is not absolute: a chloroplast can be moved to a foreign cellular environment and continue functioning for surprisingly long, given the right conditions.

The phenomenon is also a reminder that the boundary between kingdoms of life is more permeable than the schoolroom version of biology suggests. Lichens are partnerships of fungi and algae. Corals are partnerships of cnidarians and dinoflagellates. Many insects depend on bacterial endosymbionts for amino acid synthesis. Plants themselves are partnerships of eukaryotes and ancient cyanobacteria (the chloroplast) and ancient alpha-proteobacteria (the mitochondrion). The kleptoplastic sea slug is the most theatrical example of an animal becoming partly a plant, but it sits on a continuum of cross-kingdom integrations that includes much of life.

The unresolved questions about how the slug keeps the chloroplasts running for so long are an active area of research, and the answers will probably reshape some part of the textbook story about organelle dependence. The deeper observation is that biology is consistently more interconnected, more permeable, and more inventive than the categorical accounts make it sound, and a small green slug eating algae in a Massachusetts salt marsh has been quietly doing things that biologists are still working out how to explain.