Dataset Information

Functional kleptoplasts intermediate incorporation of carbon and nitrogen in cells of the Sacoglossa sea slug Elysia viridis.

ABSTRACT: 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.

SUBMITTER: Cruz S

PROVIDER: S-EPMC7324368 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Functional kleptoplasts intermediate incorporation of carbon and nitrogen in cells of the Sacoglossa sea slug Elysia viridis.

Cruz Sónia S LeKieffre Charlotte C Cartaxana Paulo P Hubas Cédric C Thiney Najet N Jakobsen Sofie S Escrig Stéphane S Jesus Bruno B Kühl Michael M Calado Ricardo R Meibom Anders A

Scientific reports 20200629 1

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 <sup>13</sup>C and <sup>15</sup>N ...[more]

PMID: 32601288

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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.

Project description:IntroductionThe Mediterranean sacoglossan Elysia timida is one of the few sea slug species with the ability to sequester chloroplasts from its food algae and to subsequently store them in a functional state in the digestive gland cells for more than a month, during which time the plastids retain high photosynthetic activity (= long-term retention). Adult E. timida have been described to feed on the unicellular alga Acetabularia acetabulum in their natural environment. The suitability of E. timida as a laboratory model culture system including its food source was studied.ResultsIn contrast to the literature reporting that juvenile E. timida feed on Cladophora dalmatica first, and later on switch to the adult diet A. acetabulum, the juveniles in this study fed directly on A. acetabulum (young, non-calcified stalks); they did not feed on the various Cladophora spp. (collected from the sea or laboratory culture) offered. This could possibly hint to cryptic speciation with no clear morphological differences, but incipient ecological differentiation. Transmission electron microscopy of chloroplasts from A. acetabulum after initial intake by juvenile E. timida showed different states of degradation - in conglomerations or singularly - and fragments of phagosome membranes, but differed from kleptoplast images of C. dalmatica in juvenile E. timida from the literature. Based on the finding that the whole life cycle of E. timida can be completed with A. acetabulum as the sole food source, a laboratory culture system was established. An experiment with PAM-fluorometry showed that cultured E. timida are also able to store chloroplasts in long-term retention from Acetabularia peniculus, which stems from the Indo-Pacific and is not abundant in the natural environment of E. timida. Variations between three experiment groups indicated potential influences of temperature on photosynthetic capacities.ConclusionsE. timida is a viable laboratory model system to study photosynthesis in incorporated chloroplasts (kleptoplasts). Capacities of chloroplast incorporation in E. timida were investigated in a closed laboratory culture system with two different chloroplast donors and over extended time periods about threefold longer than previously reported.

Dataset Information

Functional kleptoplasts intermediate incorporation of carbon and nitrogen in cells of the Sacoglossa sea slug Elysia viridis.

Publications

Functional kleptoplasts intermediate incorporation of carbon and nitrogen in cells of the Sacoglossa sea slug Elysia viridis.

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