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Chloroplast digestion and the development of functional kleptoplasty in juvenile Elysia timida (Risso, 1818) as compared to short-term and non-chloroplast-retaining sacoglossan slugs.

ABSTRACT: Sacoglossan sea slugs are the only metazoans known to perform functional kleptoplasty, the sequestration and retention of functional chloroplasts within their digestive gland cells. Remarkably, a few species with this ability can survive starvation periods of 3-12 months likely due to their stolen chloroplasts. There are no reports of kleptoplast transfer from mother slug to either eggs or juveniles, demonstrating that each animal must independently acquire its kleptoplasts and develop the ability to maintain them within its digestive gland. We present here an investigation into the development of functional kleptoplasty in a long-term kleptoplast retaining species, Elysia timida. Laboratory-reared juvenile slugs of different post-metamorphic ages were placed in starvation and compared to 5 known short-term retaining slug species and 5 non-retaining slug species. The subsequent results indicate that functional kleptoplasty is not performed by E. timida until after 15 days post-metamorphosis and that by 25 days, these animals outlive many of the short-term retention species. Digestive activity was also monitored using lysosomal abundance as an indicator, revealing different patterns in starving juveniles versus adults. Starved juveniles were reintroduced to food to determine any differences in digestive activity when starvation ends, resulting in an increase in the number of kleptoplasts, but no overall change in lysosomal activity. By revealing some of the changes that occur during early development in these animals, which begin as non-kleptoplast-retaining and grow into long-term retaining slugs, this investigation provides a basis for future inquiries into the origin and development of this remarkable ability.

SUBMITTER: Laetz EMJ

PROVIDER: S-EPMC5636068 | biostudies-other | 2017

REPOSITORIES: biostudies-other

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Chloroplast digestion and the development of functional kleptoplasty in juvenile Elysia timida (Risso, 1818) as compared to short-term and non-chloroplast-retaining sacoglossan slugs.

Laetz Elise Marie Jerschabek EMJ Wägele Heike H

PloS one 20171011 10

Sacoglossan sea slugs are the only metazoans known to perform functional kleptoplasty, the sequestration and retention of functional chloroplasts within their digestive gland cells. Remarkably, a few species with this ability can survive starvation periods of 3-12 months likely due to their stolen chloroplasts. There are no reports of kleptoplast transfer from mother slug to either eggs or juveniles, demonstrating that each animal must independently acquire its kleptoplasts and develop the abili ...[more]

PMID: 29020043

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Project description:Despite widespread interest in solar-powered sea slugs (Sacoglossa: Gastropoda), relatively little is know about how they actually perform functional kleptoplasty. Sister-taxa Elysia timida and E. cornigera provide an ideal model system for investigating this phenomenon, since they feed on the same algal genus and only E. timida is capable of long-term kleptoplasty. Recent research has explored factors regarding functional kleptoplasty in E. timida, including their starvation longevity, digestive activity, autophagal response and photosynthetic efficiency under two different temperature conditions (18 °C and 21 °C). These studies revealed the trends E. timida displays regarding each factor during starvation as well as influences temperature has on some aspects of functional kleptoplasty. This study examines E. cornigera regarding each of these factors in an attempt to elucidate differences between each species that could explain their differing kleptoplastic abilities. Since both species naturally occur in 25 °C seawater (E. timida peak summer temperature, E. cornigera low winter temperature), each species was acclimatized to 25 °C to facilitate comparison and determine if these species exhibit physiological differences to starvation when under the same environmental conditions.When comparing the different E. timida temperature treatments, it becomes clear that increased temperatures compromise E. timida's kleptoplastic abilities. Specimens acclimatized to 25 °C revealed shorter starvation longevities surviving an average 42.4 days compared to the 95.9 day average observed in specimens exposed to 18 °C. Each temperature treatment displayed a significantly different decrease throughout the starvation period in both, the rate of photosynthetic efficiency and in the decreasing functional kleptoplast abundance. Lysosomal abundances are assessed here as indicators of different aspects of metabolic activity, which could be correlated to temperature. E. cornigera, also acclimatized to 25 °C did not display significantly similar patterns as any of the E. timida temperature treatments, having fewer incorporated kleptoplasts, a higher lysosomal response to starvation, a faster decrease in photosynthetic efficiency and a lower starvation longevity.These results confirm that each species has different physiological reactions to starvation and kleptoplast retention, even under the same conditions. While temperature affects aspects of functional kleptoplasty, it is likely not responsible for the differences in kleptoplastic abilities seen in these 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.

Project description:BackgroundUnicompartmental knee arthroplasty (UKA) is an established treatment option for patients with unicompartmental osteoarthritis (OA). However, strict patient selection is crucial for its success. The proposed advantages include nearly natural knee kinematics, faster rehabilitation and better functional outcomes. Despite the aforementioned facts and it's proven cost-effectiveness, there are still hesitations for the use of UKA as an alternative to total knee arthroplasty (TKA). Key objectives of this study were therefore to assess clinical and patient-reported outcome (PRO) as well as patient's satisfaction after medial UKA in comparison to TKA.MethodsTo assess the outcome after UKA we conducted a prospective multi-center study. 116 patients with unicompartmental OA and indication for UKA were included. Overall 54 females and 62 males with an average age of 62.7 years (±9.8) and an average body mass index (BMI) of 29.2 (± 3.7) were recruited. Clinical results and PRO were assessed using the Knee Society Score (KSS). Follow-ups took place 3 months, 1 and 2 years after surgery including clinical examination, radiographs, assessment of PRO and adverse events. Pain and satisfaction was evaluated using a visual analog scale (VAS, 0 (worst) to 10 (best)). For comparison with TKA a propensity score matched-pair analysis was performed to eliminate confounders. Matching criteria were gender, patient's age, BMI and comorbidities. A total of 116 matched-pairs were analysed.ResultsThere was no revision in the UKA group until 2 years after surgery. Revision rates were higher in the TKA group (0.6%). Preoperative KSS-Scores were higher within the UKA cohort (p < 0.001). After surgical treatment, PROMs displayed a significant improvement (p < 0,001) in both cohorts. Regarding the Knee-Score (Pain, Alignment, ROM) we observed no differences between cohorts after 12 months. The Function-Score demonstrated significantly better results in the UKA cohort (UKA vs. TKA 95 vs 80, p < 0.001). Patient satisfaction was also higher in UKA patients (UKA vs TKA 9.0 vs 8.8, p = 0.019).ConclusionPatients of both cohorts showed high satisfaction after knee arthroplasty. UKA resulted in higher function scores compared to TKA without increased revision rate during short-term follow-up. Therefore, UKA is a good treatment option for unicompartmental OA.Trial registrationClinicaltrials.gov, NCT04598568 . Registered 22 October 2020 - Retrospectively registered.

Dataset Information

Chloroplast digestion and the development of functional kleptoplasty in juvenile Elysia timida (Risso, 1818) as compared to short-term and non-chloroplast-retaining sacoglossan slugs.

Publications

Chloroplast digestion and the development of functional kleptoplasty in juvenile Elysia timida (Risso, 1818) as compared to short-term and non-chloroplast-retaining sacoglossan slugs.

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