On Being the Right Size as an Animal with Plastids

Abstract

Plastids typically reside in plant or algal cells-with one notable exception. There is one group of multicellular animals, sea slugs in the order Sacoglossa, members of which feed on siphonaceous algae. The slugs sequester the ingested plastids in the cytosol of cells in their digestive gland, giving the animals the color of leaves. In a few species of slugs, including members of the genus Elysia, the stolen plastids (kleptoplasts) can remain morphologically intact for weeks and months, surrounded by the animal cytosol, which is separated from the plastid stroma by only the inner and outer plastid membranes. The kleptoplasts of the Sacoglossa are the only case described so far in nature where plastids interface directly with the metazoan cytosol. That makes them interesting in their own right, but it has also led to the idea that it might someday be possible to engineer photosynthetic animals. Is that really possible? And if so, how big would the photosynthetic organs of such animals need to be? Here we provide two sets of calculations: one based on a best case scenario assuming that animals with kleptoplasts can be, on a per cm² basis, as efficient at CO₂ fixation as maize leaves, and one based on ¹⁴CO₂ fixation rates measured in plastid-bearing sea slugs. We also tabulate an overview of the literature going back to 1970 reporting direct measurements or indirect estimates of the CO₂ fixing capabilities of Sacoglossan slugs with plastids.

Keywords: Elysia; Sacoglossa; growth rate; life cycle; photosynthetic animal; photosynthetic slugs.

Figure 1

Examples of sacoglossan sea slugs and their algal food. (A) From left to right the three Sacoglossa Elysia timida, Elysia cornigera, and Elysia viridis. All use a radula to penetrate siphonaceous algae from which they suck out the cytosolic content (hence the name sap sucking slugs) that includes compartments such as mitochondria, nuclei, and plastids. Plastids are specifically sequestered (the kleptoplasts) and incorporated into the cells that line the digestive tubules, in some cases giving the slugs their characteristic green color. The radula is a chitinous feeding structure of molluscs comparable teeth. A scanning-electron micrograph of one of E. viridis is shown on the very right, revealing the individual teeth-like structures the animals use to penetrate the algal cell wall. (B) Examples of macroalgae on which Sacoglossa feed and that are siphonacous. Some Sacoglossa are highly specialized and feed on single alga species, such as E. timida that only feeds on Acetabularia, while others such as E. viridis can feed on a larger variety of macroalgae.