KLEPTOPLASTY

History
The first reports of "green bodies" within molluscs were made in 1904 by Brüel.  However, it was not until the mid 1960's that these "green bodies" were studied and seen to be functional chloroplasts.  From this time on, there has been much interest in the phenomenon by which sea slugs find, acquire, and maintain chloroplasts as an essential component of their life-cycle.

By Elysia chlorotica
Kleptoplasty (“stealing” of chloroplasts) by Elysia chlorotica is remarkable for at least three reasons.  First, the “symbiont” in this case is not another autonomous organism with an intact genome, but rather a “naked,” foreign organelle (chloroplast). Second, the symbiont is housed intracellularly and not sequestered between cells or within a vacuolar membrane.  Third, and perhaps most remarkable, the semi-autonomous kleptoplasts remain functional for as long as ten months within the foreign host cytosol despite the absence of any of its own algal nucleo-cytosolic components.  This type of long-term activity by isolated plastids is unprecedented and astounding considering that chloroplasts are derived from once free-living cyanobacteria and have lost the majority of their genes. Hence, they are dependent on their own nucleo-cytosol for protein synthesis, targeting, and regulation of just about every function of the organelle.  In turn, chloroplasts are fragile organelles and very sensitive to physical and chemical changes in their environment, including osmotic stress.  Evidently, the advantages of photoautotrophy have provided a strong selective pressure for the evolution of this association. 

Whether the establishment of this symbiotic association is fueled by photoautotrophy pressure to sustain energy production for the sea slug when food is scarce or the need for camouflage protection when facing life without a protective shell in a predatory environment, or both, the association has not progressed to a hereditary one where the plastids are passed from one generation of slugs to the next.   Instead, the association must be established anew each year and is required for the slug to develop into a mature adult sea slug, at least in laboratory experiments.

Establishment of the Kleptoplastic Association
We have now succeeded in culturing Elysia chlorotica in the laboratory including establishing the symbiotic or kleptoplastic association with Vaucheria litorea chloroplasts. Adult E. chlorotica produce eggs, devoid of plastids, typically in late spring and planktonic veligers hatch within 4 to 5 d and then spend about 5 d feeding on unicellular algae (Rhodomonas or Isochrysis in the lab).  When subsequently provided with filaments of V. litorea, metamorphosis of the veligers into juvenile sea slugs occurs within 1 to 2 d. 

The endosymbiosis is established when young juvenile sea slugs grasp and then puncture the siphonaceous algal cells and suck out the cell contents.  All of the algal contents are “discarded” except the chloroplasts, which are engulfed phagocytotically into the digestive cells.  The captured chloroplasts fill the growing, extensively branched digestive tubules that lie just one cell layer beneath the epidermis.

Over the next several months the sea slugs may continue to feed on Vaucheria if it is available and/or sustain themselves by photoautotrophic CO2 fixation using their newly acquired chloroplasts. 



In laboratory culture, the sea slugs are kept apart from the algae, thus sustaining themselves totally by photosynthesis for up to ten months. Interestingly, death of the adults occurs almost synchronously late each spring in the lab and field (Pierce et al. 1999 Biol. Bulletin on virus).