The making of a photosynthetic animal

Abstract

Symbiotic animals containing green photobionts challenge the common perception that only plants are capable of capturing the sun's rays and converting them into biological energy through photoautotrophic CO(2) fixation (photosynthesis). 'Solar-powered' sacoglossan molluscs, or sea slugs, have taken this type of symbiotic association one step further by solely harboring the photosynthetic organelle, the plastid (=chloroplast). One such sea slug, Elysia chlorotica, lives as a 'plant' when provided with only light and air as a result of acquiring plastids during feeding on its algal prey Vaucheria litorea. The captured plastids (kleptoplasts) are retained intracellularly in cells lining the digestive diverticula of the sea slug, a phenomenon sometimes referred to as kleptoplasty. Photosynthesis by the plastids provides E. chlorotica with energy and fixed carbon for its entire lifespan of ~10 months. The plastids are not transmitted vertically (i.e. are absent in eggs) and do not undergo division in the sea slug. However, de novo protein synthesis continues, including plastid- and nuclear-encoded plastid-targeted proteins, despite the apparent absence of algal nuclei. Here we discuss current data and provide hypotheses to explain how long-term photosynthetic activity is maintained by the kleptoplasts. This fascinating 'green animal' provides a unique model to study the evolution of photosynthesis in a multicellular heterotrophic organism.

Fig. 1.

Examples of diverse photosynthetic animals with varied symbionts. (A) Neopetrosia subtriangularis with Synechococcus (photo by Robert Thacker); (B) Didemnum molle with Prochloron (inset) (photo by Euichi Hirose); (C) Symsagittifera sp. with Tetraselmis symbionts [modified here from fig. 1 in Hooge and Tyler (Hooge and Tyler, 2008), with permission of Magnolia Press]; (D) Cassiopea xamachana with Symbiodinium (photo by Alan Verde); (E) green Hydra with Chlorella (photo by Thomas Bosch); (F) confocal image of Fungia coral larva (blue) with red autofluorescent Symbiodinium (photo by Virginia Weis); and (G) Tridacna spp. with Symbiodinium (photo by Jesús Pineda with permission from Woods Hole Oceanographic Institution).

Fig. 2.

Examples of photosynthetic sacoglossans with varied times of chloroplast retention. (A) Elysia chlorotica [reprinted with permission (Rumpho et al., 2008)], (B) Elysia crispata, (C) Plakobranchus ocellatus, (D) Costasiella ocellifera, (E) Thuridilla gracilis, (F) Costasiella kurishimae, (G) Alderia modesta, (H) Lobiger viridis and (I) Oxynoe antillarum. Photos in panels B, D, E, G and I were provided with permission by Patrick Krug; photos in panels C, F and H were provided with permission by Heike Wägele.

Fig. 3.

Evolutionary scheme for primary, secondary and tertiary plastids. The secondary endosymbiotic origin of plastids is illustrated in Vaucheria litorea from the red algal lineage. The subsequent acquisition of V. litorea plastids by the sea slug Elysia chlorotica in a tertiary endosymbiotic event imparts photosynthetic activity to this heterotroph.

Fig. 4.

Life cycle of Elysia chlorotica. After 4 days, veliger larvae hatch from egg ribbons and live planktonically for 3 weeks until competent for metamorphosis. Upon detection of the algal prey Vaucheria litorea, mature veligers settle out of the water onto the algal filaments and metamorphose into juvenile sea slugs. Feeding occurs immediately and plastids are observed inside the animal within 24 h of settlement and metamorphosis. After continual feeding of 5 to 7 days, the association becomes permanent and the plastids are stable within the animal. Additional feeding leads to growth of the juvenile to the adult stage and further incorporation of plastids into the animal tissues. Adults live for ∼10 months in the wild, senescing often after mating in the spring.

Fig. 5.

Schematic of the light and dark reactions of photosynthesis showing plastid- vs nuclear-encoded genes. (A) Adult, kleptoplastic Elysia chlorotica. (B) Transmission electron micrograph showing numerous algal plastids within a cell lining the digestive diverticuli of the sea slug. (C,D) Schematic of the two photosynthetic processes overlaid on a plastid illustrating the essential proteins required in each pathway. Nuclear-encoded plastid proteins are shaded blue for both the electron transfer chain (C) and the Calvin–Bensen cycle (D). In the latter, RuBisCO is shaded green to indicate a plastid-encoded protein. Two of the enzymes, phosphoribulokinase and sedoheptulose-1,7-bisphosphatase, are shaded dark blue to indicate that, although they are nuclear-encoded like the light-blue-shaded enzymes, these enzymes are unique to phototrophs and are not typically found in an animal, whereas the light-blue-shaded enzymes all have homologs in animal metabolism.