Mollusc-Algal Chloroplast Endosymbiosis. Photosynthesis, Thylakoid Protein Maintenance, and Chloroplast Gene Expression Continue for Many Months in the Absence of the Algal Nucleus

Abstract

Early in its life cycle, the marine mollusc Elysia chlorotica Gould forms an intracellular endosymbiotic association with chloroplasts of the chromophytic alga Vaucheria litorea C. Agardh. As a result, the dark green sea slug can be sustained in culture solely by photoautotrophic CO 2 fixation for at least 9 months if provided with only light and a source of CO 2 . Here we demonstrate that the sea slug symbiont chloroplasts maintain photosynthetic oxygen evolution and electron transport activity through photosystems I and II for several months in the absence of any external algal food supply. This activity is correlated to the maintenance of functional levels of chloroplast-encoded photosystem proteins, due in part at least to de novo protein synthesis of chloroplast proteins in the sea slug. Levels of at least one putative algal nuclear encoded protein, a light-harvesting complex protein homolog, were also maintained throughout the 9-month culture period. The chloroplast genome of V. litorea was found to be 119.1 kb, similar to that of other chromophytic algae. Southern analysis and polymerase chain reaction did not detect an algal nuclear genome in the slug, in agreement with earlier microscopic observations. Therefore, the maintenance of photosynthetic activity in the captured chloroplasts is regulated solely by the algal chloroplast and animal nuclear genomes.

Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica

“…Likewise, animal genomes have never been shown to contain psbO; hence, MSP cannot be made by the sea slug in the absence of HGT. We have previously demonstrated that oxygen evolution is linked to photosynthetic electron transport in the sea slug for at least 5 months after being removed from its algal prey (27), and photosystem II is generally highly susceptible to photo-oxidative damage requiring de novo synthesis and reassembly of its subunits (38,39). For these reasons, we targeted psbO for HGT from V. litorea to E. chlorotica.…”

“…This emerald green sea slug owes its coloring and photosynthetic ability to plastids acquired during herbivorous feeding (24)(25)(26)(27)(28)(29). The plastids do not undergo division in the sea slug and are sequestered intracellularly in cells lining the finely divided digestive diverticula.…”

“…The plastids do not undergo division in the sea slug and are sequestered intracellularly in cells lining the finely divided digestive diverticula. The plastids continue to carry out photosynthesis, providing the sea slug with energy and carbon during its approximately 10-month life span (27,28). Long-term plastid activity continues despite the absence of algal nuclei (27,29), and hence a source of nuclear-encoded plastid-targeted proteins.…”

“…The plastids continue to carry out photosynthesis, providing the sea slug with energy and carbon during its approximately 10-month life span (27,28). Long-term plastid activity continues despite the absence of algal nuclei (27,29), and hence a source of nuclear-encoded plastid-targeted proteins. We hypothesize that the algal nuclear genes encoding essential plastid proteins are present in the sea slug, presumably as a result of HGT.…”

Elysiapyrones from Elysia diomedea. Do Such Metabolites Evidence an Enzymatically Assisted Electrocyclization Cascade for the Biosynthesis of Their Bicyclo[4.2.0]octane Core?

“…1 While the plastids remain photosynthetically active they provide an energy supply, and in some cases, the released organic carbon can totally sustain the sea slugs for several months in the absence of an algal food source, 2 giving rise to the issue of whether lateral gene transfer has occurred between eukaryotic alga and animal † Instituto de Productos Naturales y Agrobiología del CSIC. ‡ Smithsonian Tropical Research Institute.…”