Crawling leaves: photosynthesis in sacoglossan sea slugs

By Sónia Cruz

“Crawling leaves” or “solar-powered sea slugs” are common terms used to name some species of sacoglossan sea slugs capable of performing photosynthesis, a process usually associated with plants. These sea slugs ingest macroalgal tissue and retain undigested functional chloroplasts in special cells of their gut (kleptoplasty). The “stolen” chloroplasts (kleptoplasts) continue to photosynthesize, in some cases up to one year.

While kleptoplasty has been known about for over a century, the mechanisms of interaction between the kleptoplasts and its host animal cell are just now starting to be unravelled. Particularly puzzling is the maintenance of photosynthetic activity in the absence of an algal nucleus, considering the fact that the chloroplast genome is expected to encode only a small fraction of the proteins considered necessary for photosynthesis.

Our study, published in the Journal of Experimental Botany, reviews the following affairs regarding sacoglossan sea slugs:

1. The use of light energy sources to make the complex organic molecules that we call food, from inorganic substances (photosynthesis as an autotrophic nutritional source);
2. Animal responses to light in relation to what is going on in the kleptoplasts (photobiology);
3. Advantages and drawbacks of using a non-invasive technique which indirectly addresses photosynthesis, termed pulse amplitude modulated (PAM) fluorometry, in the study of in vivo photobiology in these organisms.

Several studies have shown the importance of photosynthesis on the nutrition of photosynthetic sea slugs kept in the laboratory and deprived of exogenous food sources. Much fewer studies have unequivocally demonstrated the importance of autotrophy on the nutritional state of natural populations of photosynthetic sea slugs.

In the study of sacoglossan sea slugs as photosynthetic systems, it is important to understand their relationship with light. On one hand, these organisms seem to move towards light, possibly to increase light harvesting at the kleptoplast level. On the other hand, sacoglossan sea slugs seem to avoid high light intensities, possibly as a strategy to avoid the damage that excessive light can cause to the kleptoplasts (photoinhibition) and, in this way, prevent premature loss of kleptoplast photosynthetic function.

We have previously shown that the longevity of kleptoplasts in the sea slug Elysia viridis present in the Atlantic coast of mainland Portugal depends greatly on the light intensity to which animals are exposed, with premature loss of photosynthetic activity occurring under higher light intensities. This is one of the many factors that can lead to data misinterpretation, including in the attempt to rank longevity of kleptoplast retention. In our review, we revisit the strategies developed by plants and algae to avoid excessive light, with emphasis on the physiological and behavioural mechanisms suggested to be involved in the protection of kleptoplasts from high light intensities.

A particularly specialized behaviour in response to light has been proposed for the sea slug Elysia timida: this species may use the lateral body flaps (parapodia) to control exposure of kleptoplasts to light, opening their parapodia wide (‘fully spread posture resembling a flattened leaf’) under lower light intensities and closing them (‘contracted or arrow-like form’) at higher intensities. This ‘behavioural photoprotection’ strategy is yet to be demonstrated for other photosynthetic sea slug species with parapodia.

We gave a special focus to the advantages and drawbacks of using PAM fluorometry in the study of in vivo photosynthesis in sacoglossan sea slugs. This non-intrusive technique was developed for research in plant physiology and the problems associated with motile animals are often disregarded. Finally, the review briefly discusses the importance of culturing these organisms in the laboratory in order to control certain key factors such as age, fitness, previous food habits, and acclimation to different light intensities in specimens used for experimental trials.

Sónia Cruz was awarded a PhD from the University of Sheffield and has worked in four different labs across Europe: Horton Lab in Sheffield, Wilhelm Lab at Leipzig University, Smith Lab at Cambridge University, and finally, at her home country, Serôdio Lab at Aveiro University in Portugal. Having worked on algae physiology for the last 8 years, she recently became interested in the fascinating symbiosis between a mollusk and algae chloroplasts. In 2012, Sónia was awarded a Marie Curie Career Integration Grant. She is the co-author of the paper ‘Crawling leaves: photosynthesis in sacoglossan sea slugs‘, which is published in the Journal of Experimental Botany.

The aim of the Journal of Experimental Botany is to publish the highest quality manuscripts that address questions of broad interest in plant biology.

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Image credit: The picture first appeared online in the article ‘Crawling leaves: photosynthesis in sacoglossan sea slugs‘, published in the Journal of Experimental Botany. © Oxford University Press, 2013. Do not use without permission.