Abstract:The establishment of kleptoplasty (retention of “stolen plastids”) in the digestive tissue of the sacoglossan Elysia chlorotica Gould was investigated using transmission electron microscopy. Cellular processes occurring during the initial exposure to plastids were observed in laboratory raised animals ranging from 1–14 days post metamorphosis (dpm). These observations revealed an abundance of lipid droplets (LDs) correlating to plastid abundance. Starvation of animals resulted in LD and plastid decay in animal… Show more
“…In E. timida , we observed a similar, yet less steep, decline in the concentration of pigments in relation to body mass over the 10 days of starvation measured (from 2193 to 1606 at day 4 (73.2%) and 1638 pmol Chl a + b /mg animal dry weight at day 10 (74.7%); figure 1 b ). The increase of photosynthesis-associated pigments around day 6 demonstrates that the animals we measured metabolize their own tissue at an apparently faster rate than the kleptoplasts degrade, which was also observed for starving juveniles of E. chlorotica [23]. Figure 1. Elysia cornigera dies while showing comparable photosynthetic activity to E. timida during starvation.…”
The only animal cells known that can maintain functional plastids (kleptoplasts) in their cytosol occur in the digestive gland epithelia of sacoglossan slugs. Only a few species of the many hundred known can profit from kleptoplasty during starvation long-term, but why is not understood. The two sister taxa Elysia cornigera and Elysia timida sequester plastids from the same algal species, but with a very different outcome: while E. cornigera usually dies within the first two weeks when deprived of food, E. timida can survive for many months to come. Here we compare the responses of the two slugs to starvation, blocked photosynthesis and light stress. The two species respond differently, but in both starvation is the main denominator that alters global gene expression profiles. The kleptoplasts' ability to fix CO2 decreases at a similar rate in both slugs during starvation, but only E. cornigera individuals die in the presence of functional kleptoplasts, concomitant with the accumulation of reactive oxygen species (ROS) in the digestive tract. We show that profiting from the acquisition of robust plastids, and key to E. timida's longer survival, is determined by an increased starvation tolerance that keeps ROS levels at bay.
“…In E. timida , we observed a similar, yet less steep, decline in the concentration of pigments in relation to body mass over the 10 days of starvation measured (from 2193 to 1606 at day 4 (73.2%) and 1638 pmol Chl a + b /mg animal dry weight at day 10 (74.7%); figure 1 b ). The increase of photosynthesis-associated pigments around day 6 demonstrates that the animals we measured metabolize their own tissue at an apparently faster rate than the kleptoplasts degrade, which was also observed for starving juveniles of E. chlorotica [23]. Figure 1. Elysia cornigera dies while showing comparable photosynthetic activity to E. timida during starvation.…”
The only animal cells known that can maintain functional plastids (kleptoplasts) in their cytosol occur in the digestive gland epithelia of sacoglossan slugs. Only a few species of the many hundred known can profit from kleptoplasty during starvation long-term, but why is not understood. The two sister taxa Elysia cornigera and Elysia timida sequester plastids from the same algal species, but with a very different outcome: while E. cornigera usually dies within the first two weeks when deprived of food, E. timida can survive for many months to come. Here we compare the responses of the two slugs to starvation, blocked photosynthesis and light stress. The two species respond differently, but in both starvation is the main denominator that alters global gene expression profiles. The kleptoplasts' ability to fix CO2 decreases at a similar rate in both slugs during starvation, but only E. cornigera individuals die in the presence of functional kleptoplasts, concomitant with the accumulation of reactive oxygen species (ROS) in the digestive tract. We show that profiting from the acquisition of robust plastids, and key to E. timida's longer survival, is determined by an increased starvation tolerance that keeps ROS levels at bay.
“…It is also still unclear whether any photosynthates produced are immediately transported to the slug or if the slug lacks the feedback system found in the algae, therefore directly causing a build up of starch within the kleptoplast. Any starch build up would support the more recent “larder hypothesis” [25, 32] - that photosynthesis does contribute to meeting a starving slug’s metabolic needs, but not through the continuous release of the photosynthates produced, but rather by storing them inside the plastid where they later become available to the slug when the plastids are finally digested at a later time point.…”
Section: Introductionmentioning
confidence: 64%
“…Recent hypotheses consider sequestered chloroplasts as a source of stored food reserves rather than as a source of directly and continuously available photosynthates [24, 25]. …”
Section: Introductionmentioning
confidence: 99%
“…Pelletreau et al [25] observed lipid droplet accumulation in E. chlorotica’s digestive gland tubules during a starvation period, and they state that these lipid droplets were likely “of algal origin”. Lipid droplets are known to be the main photosynthate storage molecule produced by V. litorea , so this accumulation is not surprising and lends evidence to the hypothesis regarding chloroplasts as photosynthate larders.…”
BackgroundSolar-powered sea slugs are famed for their ability to survive starvation due to incorporated algal chloroplasts. It is well established that algal-derived carbon can be traced in numerous slug-derived compounds, showing that slugs utilize the photosynthates produced by incorporated plastids. Recently, a new hypothesis suggests that the photosynthates produced are not continuously made available to the slug. Instead, at least some of the plastid’s photosynthetic products are stored in the plastid itself and only later become available to the slug. The long-term plastid-retaining slug, Elysia timida and its sole food source, Acetabularia acetabulum were examined to determine whether or not starch, a combination of amylose and amylopectin and the main photosynthate produced by A. acetabulum, is produced by the stolen plastids and whether it accumulates within individual kleptoplasts, providing an energy larder, made available to the slug at a later time.ResultsHistological sections of Elysia timida throughout a starvation period were stained with Lugol’s Iodine solution, a well-known stain for starch granules in plants. We present here for the first time, an increase in amylose concentration, within the slug’s digestive gland cells during a starvation period, followed by a sharp decrease. Chemically blocking photosynthesis in these tissues resulted in no observable starch, indicating that the starch in untreated animals is a product of photosynthetic activity.ConclusionThis suggests that kleptoplasts function as both, a nutritive producer and storage device, holding onto the polysaccharides they produce for a certain time until they are finally available and used by the starving slug to withstand extended starvation periods.
“…Acquiring symbionts horizontally always includes an aposymbiotic life stage present in all photosymbiotic animal lineages, which is usually the larval phase before metamorphosis into juveniles (e.g. Belda‐Baillie et al, ; Weis et al, ; Harrison, ; Pelletreau et al, ; Mies et al, ). Juveniles then successfully take up the symbiont from their environment, but there seems to be little co‐evolution of species with horizontal transmission and their symbiont partners (van Oppen et al, ; Bright & Bulgheresi, ).…”
Section: Evolutionary Genomics Of Photosymbiosesmentioning
Mutualistic symbioses are common throughout the animal kingdom. Rather unusual is a form of symbiosis, photosymbiosis, where animals are symbiotic with photoautotrophic organisms. Photosymbiosis is found among sponges, cnidarians, flatworms, molluscs, ascidians and even some amphibians. Generally the animal host harbours a phototrophic partner, usually a cyanobacteria or a unicellular alga. An exception to this rule is found in some sea slugs, which only retain the chloroplasts of the algal food source and maintain them photosynthetically active in their own cytosol - a phenomenon called 'functional kleptoplasty'. Research has focused largely on the biodiversity of photosymbiotic species across a range of taxa. However, many questions with regard to the evolution of the ability to establish and maintain a photosymbiosis are still unanswered. To date, attempts to understand genome adaptations which could potentially lead to the evolution of photosymbioses have only been performed in cnidarians. This knowledge gap for other systems is mainly due to a lack of genetic information, both for non-symbiotic and symbiotic species. Considering non-photosymbiotic species is, however, important to understand the factors that make symbiotic species so unique. Herein we provide an overview of the diversity of photosymbioses across the animal kingdom and discuss potential scenarios for the evolution of this association in different lineages. We stress that the evolution of photosymbiosis is probably based on genome adaptations, which (i) lead to recognition of the symbiont to establish the symbiosis, and (ii) are needed to maintain the symbiosis. We hope to stimulate research involving sequencing the genomes of various key taxa to increase the genomic resources needed to understand the most fundamental question: how have animals evolved the ability to establish and maintain a photosymbiosis?
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