Datasets accompanying the manuscript: "Food shaped photosynthesis: Photophysiology of the sea slug Elysia viridis fed with two alternative chloroplast donors"
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ABSTRACT:
ORGANISM(S): Elysia viridis Chaetomorpha Codium tomentosum
SUBMITTER:
PROVIDER: S-BSST1106 | biostudies-other |
REPOSITORIES: biostudies-other
Similar Datasets
Project description:Several sacoglossan sea slug species feed on macroalgae and incorporate chloroplasts into tubular cells of their digestive diverticula. We investigated the role of the "stolen" chloroplasts (kleptoplasts) in the nutrition of the sea slug Elysia viridis and assessed how their abundance, distribution and photosynthetic activity were affected by light and starvation. Elysia viridis individuals feeding on the macroalga Codium tomentosum were compared with starved specimens kept in dark and low light conditions. A combination of variable Chl a fluorescence and hyperspectral imaging, and HPLC pigment analysis was used to evaluate the spatial and temporal variability of photopigments and of the photosynthetic capacity of kleptoplasts. We show increased loss of weight and body length in dark-starved E. viridis as compared to low light-starved sea slugs. A more pronounced decrease in kleptoplast abundance and lower photosynthetic electron transport rates were observed in dark-starved sea slugs than in low light-starved animals. This study presents strong evidence of the importance of kleptoplast photosynthesis for the nutrition of E. viridis in periods of food scarcity. Deprived of photosynthates, E. viridis could accelerate the breakdown of kleptoplasts in the dark to satisfy its' energy requirements.
| S-EPMC5552801 | biostudies-other
Project description:Photosynthesis is a fundamental process sustaining heterotrophic organisms at all trophic levels. Some mixotrophs can retain functional chloroplasts from food (kleptoplasty), and it is hypothesized that carbon acquired through kleptoplasty may enhance trophic energy transfer through increased host growth efficiency. Sacoglossan sea slugs are the only known metazoans capable of kleptoplasty, but the relative fitness contributions of heterotrophy through grazing, and phototrophy via kleptoplasts, are not well understood. Fitness benefits (i.e. increased survival or growth) of kleptoplasty in sacoglossans are commonly studied in ecologically unrealistic conditions under extended periods of complete darkness and/or starvation. We compared the growth efficiency of the sacoglossan Elysia viridis with access to algal diets providing kleptoplasts of differing functionality under ecologically relevant light conditions. Individuals fed Codium fragile, which provide highly functional kleptoplasts, nearly doubled their growth efficiency under high compared to low light. In contrast, individuals fed Cladophora rupestris, which provided kleptoplasts of limited functionality, showed no difference in growth efficiency between light treatments. Slugs feeding on Codium, but not on Cladophora, showed higher relative electron transport rates (rETR) in high compared to low light. Furthermore, there were no differences in the consumption rates of the slugs between different light treatments, and only small differences in nutritional traits of algal diets, indicating that the increased growth efficiency of E. viridis feeding on Codium was due to retention of functional kleptoplasts. Our results show that functional kleptoplasts from Codium can provide sacoglossan sea slugs with fitness advantages through photosynthesis.
| S-EPMC4382131 | biostudies-literature
Project description:Some sacoglossan sea slugs incorporate intracellular functional algal chloroplasts, a process termed kleptoplasty. "Stolen" chloroplasts (kleptoplasts) can remain photosynthetically active up to several months, contributing to animal nutrition. Whether this contribution occurs by means of translocation of photosynthesis-derived metabolites from functional kleptoplasts to the animal host or by simple digestion of such organelles remains controversial. Imaging of 13C and 15N assimilation over a 12-h incubation period of Elysia viridis sea slugs showed a light-dependent incorporation of carbon and nitrogen, observed first in digestive tubules and followed by a rapid accumulation into chloroplast-free organs. Furthermore, this work revealed the presence of 13C-labeled long-chain fatty acids (FA) typical of marine invertebrates, such as arachidonic (20:4n-6) and adrenic (22:4n-6) acids. The time frame and level of 13C- and 15N-labeling in chloroplast-free organs indicate that photosynthesis-derived primary metabolites were made available to the host through functional kleptoplasts. The presence of specific 13C-labeled long-chain FA, absent from E. viridis algal food, indicates animal based-elongation using kleptoplast-derived FA precursors. Finally, carbon and nitrogen were incorporated in organs and tissues involved in reproductive functions (albumin gland and gonadal follicles), implying a putative role of kleptoplast photosynthesis in the reproductive fitness of the animal host.
| S-EPMC7324368 | biostudies-literature
Project description:Sacoglossan sea slugs, also known as crawling leaves due to their photosynthetic activity, are highly selective feeders that incorporate chloroplasts from specific macroalgae. These "stolen" plastids - kleptoplasts - are kept functional inside animal cells and likely provide an alternative source of energy to their host. The mechanisms supporting the retention and functionality of kleptoplasts remain unknown. A lipidomic mass spectrometry-based analysis was performed to study kleptoplasty of the sacoglossan sea slug Elysia viridis fed with Codium tomentosum. Total lipid extract of both organisms was fractionated. The fraction rich in glycolipids, exclusive lipids from chloroplasts, and the fraction rich in betaine lipids, characteristic of algae, were analysed using hydrophilic interaction liquid chromatography-mass spectrometry (HILIC-LC-MS). This approach allowed the identification of 81 molecular species, namely galactolipids (8 in both organisms), sulfolipids (17 in C. tomentosum and 13 in E. viridis) and betaine lipids (51 in C. tomentosum and 41 in E. viridis). These lipid classes presented similar lipidomic profiles in C. tomentosum and E. viridis, indicating that the necessary mechanisms to perform photosynthesis are preserved during the process of endosymbiosis. The present study shows that there are no major shifts in the lipidome of C. tomentosum chloroplasts sequestered by E. viridis.
| S-EPMC5597624 | biostudies-literature
Project description:Long-term retention of functional chloroplasts in animal cells occurs only in sacoglossan sea slugs. Analysis of molecules related to the maintenance of these organelles can provide valuable information on this trait (kleptoplasty). The goal of our research was to characterize the pigment and fatty acid (FA) composition of the sea slug Elysia crispata and their associated chloroplasts that are kept functional for a long time, and to quantify total lipid, glycolipid and phospholipid contents, identifying differences between habitats: shallow (0-4 m) and deeper (8-12 m) waters. Specimens were sampled and analyzed after a month of food deprivation, through HPLC, GC-MS and colorimetric methods, to ensure an assessment of long-term kleptoplasty in relation to depth. Pigment signatures indicate that individuals retain chloroplasts from different macroalgal sources. FA classes, phospholipid and glycolipid contents displayed dissimilarities between depths. However, heterogeneities in pigment and FA profiles, as well as total lipid, glycolipid and phospholipid amounts in E. crispata were not related to habitat depth. The high content of chloroplast origin molecules, such as Chl a and glycolipids after a month of starvation, confirms that E. crispata retains chloroplasts in good biochemical condition. This characterization fills a knowledge gap of an animal model commonly employed to study kleptoplasty.
| S-EPMC8614334 | biostudies-literature
Project description:Elysia chlorotica, a sacoglossan sea slug found off the East Coast of the United States, is well-known for its ability to sequester chloroplasts from its algal prey and survive by photosynthesis for up to 12 months in the absence of food supply. Here we present a draft genome assembly of E. chlorotica that was generated using a hybrid assembly strategy with Illumina short reads and PacBio long reads. The genome assembly comprised 9,989 scaffolds, with a total length of 557?Mb and a scaffold N50 of 442?kb. BUSCO assessment indicated that 93.3% of the expected metazoan genes were completely present in the genome assembly. Annotation of the E. chlorotica genome assembly identified 176?Mb (32.6%) of repetitive sequences and a total of 24,980 protein-coding genes. We anticipate that the annotated draft genome assembly of the E. chlorotica sea slug will promote the investigation of sacoglossan genetics, evolution, and particularly, the genetic signatures accounting for the long-term functioning of algal chloroplasts in an animal.
| S-EPMC6380222 | biostudies-literature
Project description:The sea slug Elysia chlorotica acquires plastids by ingestion of its algal food source Vaucheria litorea. Organelles are sequestered in the mollusc's digestive epithelium, where they photosynthesize for months in the absence of algal nucleocytoplasm. This is perplexing because plastid metabolism depends on the nuclear genome for >90% of the needed proteins. Two possible explanations for the persistence of photosynthesis in the sea slug are (i) the ability of V. litorea plastids to retain genetic autonomy and/or (ii) more likely, the mollusc provides the essential plastid proteins. Under the latter scenario, genes supporting photosynthesis have been acquired by the animal via horizontal gene transfer and the encoded proteins are retargeted to the plastid. We sequenced the plastid genome and confirmed that it lacks the full complement of genes required for photosynthesis. In support of the second scenario, we demonstrated that a nuclear gene of oxygenic photosynthesis, psbO, is expressed in the sea slug and has integrated into the germline. The source of psbO in the sea slug is V. litorea because this sequence is identical from the predator and prey genomes. Evidence that the transferred gene has integrated into sea slug nuclear DNA comes from the finding of a highly diverged psbO 3' flanking sequence in the algal and mollusc nuclear homologues and gene absence from the mitochondrial genome of E. chlorotica. We demonstrate that foreign organelle retention generates metabolic novelty ("green animals") and is explained by anastomosis of distinct branches of the tree of life driven by predation and horizontal gene transfer.
| S-EPMC2584685 | biostudies-literature
Project description:Elysia crispata is a tropical sea slug Sacoglossa is a superorder of marine sea slugs, of which a few speciesthat can retain intracellular functional chloroplasts from their its algae prey, a mechanism termed kleptoplasty. Elysia crispata is a tropical species of Sacoglossa that can feed through this mechanism on and acquire chloroplasts from a variety of macroalgae. Thisese sea slugs, as other gastropods, produce mucus, a viscous secretion with multiple functions, such as lubrication, protection, and locomotion. This study presents the first comprehensive analysis of the mucus proteome of the sea slug E. crispata using gel electrophoresis and HPLC-MS/MS. We identified 306 proteins in the mucus secretions of this animal, despite the limited entries for E. crispata in the Uniprot database. The reproducibility of the mucus sampling technique was evaluated revealing no significant differences in protein abundance across samples. The functional annotation of the mucus proteome using Gene Ontology identified proteins involved in different functions such as hydrolase activity (molecular function), carbohydrate-derived metabolic processes (biological processes) and cytoskeletal organization (cell component). Moreover, a high proportion of proteins with enzymatic activity in the mucus of E. crispata suggests potential biotechnological applications including antimicrobial and antitumor activities. Putative antimicrobial properties are reinforced by the high abundance of hydrolases. This study also identified proteins common in mucus samples from various species, supporting a common mechanism of mucus in protecting cells and tissues while facilitating animal movement. This study highlights the need for further research to fully understand the roles of these proteins in mucus, their potential impact on animal physiology, and the influence of genetics, and environmental factors, including the type of mucus, on protein composition and relative abundance.
2024-01-22 | PXD042643 | Pride
Project description:Thioredoxins (TRXs) are protein oxidoreductases that control the structure and function of cellular proteins by cleavage of a disulphide bond between the side chains of two cysteine residues. Oxidized thioredoxins are reactivated by thioredoxin reductases (TR) and a TR-dependent reduction of TRXs is called a thioredoxin system. Thiol-based redox regulation is an especially important mechanism to control chloroplast proteins involved in biogenesis, in regulation of light harvesting and distribution of light energy between photosystems, in photosynthetic carbon fixation and other biosynthetic pathways, and in stress responses of plants. Of the two plant plastid thioredoxin systems, the ferredoxin-dependent system relays reducing equivalents from photosystem I via ferredoxin and ferredoxin-thioredoxin reductase (FTR) to chloroplast proteins, while NADPH-dependent thioredoxin reductase (NTRC) forms a complete thioredoxin system including both reductase and thioredoxin domains in a single polypeptide. Chloroplast thioredoxins transmit environmental light signals to biochemical reactions, which allows fine tuning of photosynthetic processes in response to changing environmental conditions. In this paper we focus on the recent reports on specificity and networking of chloroplast thioredoxin systems and evaluate the prospect of improving photosynthetic performance by modifying the activity of thiol regulators in plants.This article is part of the themed issue 'Enhancing photosynthesis in crop plants: targets for improvement'.
| S-EPMC5566889 | biostudies-other
Project description:BACKGROUND: In simultaneous hermaphrodites with copulation and internal fertilization it is often unclear whether reciprocal sperm exchange results from the unconditional willingness of both partners to donate and receive sperm, or whether it follows from a more controlled process such as conditional reciprocal sperm exchange, i.e. sperm trading. While in some sea slugs mating is assumed to be based on sperm trading, it seems to be unconditional in others. Here, we describe the unusual mating behaviour of Elysia timida, a small sacoglossan, focussing on indications for conditional reciprocity. RESULTS: E. timida shows an as yet unique combination of a long series of hypodermic transfers followed by a short phase with standard insemination into a female genital aperture. Hypodermic transfer takes place in the form of repeated small injections into the dorsal surface of the partner, interrupted by synchronised circling movements. In the final mating phase sperm is transferred into the female genital aperture in a short period. In both phases the two mating individuals show a high degree of transfer symmetry and synchrony. While total duration and number of transfers were balanced within pairs, they varied significantly between pairs. Furthermore, looking at individual hypodermic transfers within pairs, reciprocal transfers lasted longer than unilateral transfers. Final sperm transfers were always reciprocal except for two cases which also diverted from the usual pattern in ways that were suggestive of a conflict over reciprocity. CONCLUSION: Our results suggest that individual mating decisions in E. timida depend on what the partner does, indicating conditional reciprocity. If hypodermic transfers also involve the transfer of sperm (which remains to be confirmed), this system represents an up to now unique transition stage between hypodermic and standard insemination, both of which are widespread in this group of sea slugs, but never have been observed to co-occur within the same species.
| S-EPMC1934903 | biostudies-other