Provision of phosphates by the host supports kleptoplast functionality in photosynthetic sea slugs

Phosphorus and nitrogen are two fundamental macronutrients needed for photosynthesis, and their balance in photosymbiotic relationships, like those between corals and their zooxanthellae, is known to be highly important for maintaining a healthy partnership between the host and the symbiont. Kleptoplasty is a special case of algae-herbivore interaction, where the host animal or protist sequesters the chloroplasts from their prey algae as kleptoplasts inside their own cells. In some kleptoplastic sea slugs, the kleptoplasts can remain functional for months without the help from the algal nucleus, and the fundamental mechanisms in place to achieve this are still largely unsolved. Unlike in purely symbiotic systems like corals, the importance of nutrient balance to kleptoplast longevity has not been addressed in kleptoplastic sea slugs. We studied the phosphate and nitrogen exchange between the sea slug Elysia timida and its Acetabularia acetabulum derived kleptoplasts in various nutrient depletion and replenishment experiments. Our results show that sea slugs consumed phosphate from their surrounding medium and were able to recover electron transfer rates of kleptoplasts originating from phosphate depleted algae, suggesting that the sea slug provided the acquired organelles with phosphate to the extent that they increased the photosynthetic capacity remarkably well. Additional available phosphate in the water also increased the overall longevity of the kleptoplasts. The sea slugs were not able to recover the photosynthesis of nitrogen-depleted kleptoplasts, and additional dissolved nitrate and ammonium were not beneficial for kleptoplast longevity. Our results suggest that the phosphate-nitrogen balance inside the sea slug cells is mainly limited by phosphate, the addition of which can help the kleptoplasts maintain photosynthesis, perhaps by allowing the use of the glutamine synthetase (GS) and glutamate synthase (GOGAT) nitrogen assimilation pathway to function as an efficient alternative electron sink.