Summary: | The vulnerability of marine photosynthetic symbioses to climate-driven changes has deserved particular attention in recent years. However, while there is an increasing number of studies on emblematic species such as symbiotic corals, little is known about less charismatic groups such as solar-powered sea slugs. These organisms display one of the most puzzling features observed in the animal kingdom: the mollusc-plastid association, which results from their ability to retain photosynthetically active chloroplasts (kleptoplasts) “stolen” from their algal food sources. Given their peculiar biology, sea slugs have stood out as tool organisms for academic research on photobiology, biomedical studies and bioprospecting of new marine drugs, becoming also desired critters in the marine aquarium trade. In order to provide an overview of state-of-the-art on our knowledge on these fascinating organisms, and lay down the foundations for climate change research, the biological and ecological features of the mollusc-plastid association were reviewed and optimal culture conditions for their different life stages were identified. The impact of ocean acidification and warming was evaluated on early stages and adults of temperate (Elysia viridis) and tropical (Elysia clarki) sea slugs. In this context, new methodological approaches were developed to non-invasively assess the photophysiology of kleptoplasts under future ocean conditions. Our results have shown that acidification and warming may impact several biological features of solar-powered sea slugs, including survival, reproductive success, growth, incidence of deformities, kleptoplasts photosynthetic efficiency, metabolism, heat shock and antioxidant responses. However, sea slug tolerance to future ocean conditions was shown to be species-specific. The temperate sea slug E. viridis, in spite of their low survival, presented efficient heat shock and antioxidant defence mechanisms and high rates of photosynthesis and respiration when exposed to acidification and warming, suggesting the existence of a more tolerant mollusc-kleptoplast complex and capacity to cope with future scenarios. In contrast, the tropical sea slug E. clarki showed to be quite vulnerable to future ocean conditions. The reduced capacity or lack of mechanisms to deal with environmental stress may, in part, explain the metabolic depression of the holobiont and the reduced photosynthetic efficiency of kleptoplasts, leading to bleaching and a lower survival. This work is the first reporting the occurrence of bleaching under climate change in other photosynthetic symbiosis than the cnidarian-dinoflagellate association. These results have broad implications and may help us to anticipate potential negative impacts on the recruitment of solar-powered sea slugs in the oceans of tomorrow. However, it is worth noting that solar-powered sea slugs may have time and evolutionary opportunities to adapt to future ocean conditions.
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