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1.
Kleptoplasty is a remarkable type of photosynthetic association, resulting from the maintenance of functional chloroplasts—the ‘kleptoplasts’—in the tissues of a non-photosynthetic host. It represents a biologically unique condition for chloroplast and photosynthesis functioning, occurring in different phylogenetic lineages, namely dinoflagellates, ciliates, foraminiferans and, most interestingly, a single taxon of metazoans, the sacoglossan sea slugs. In the case of sea slugs, chloroplasts from macroalgae are often maintained as intracellular organelles in cells of these marine gastropods, structurally intact and photosynthetically competent for extended periods of time. Kleptoplasty has long attracted interest owing to the longevity of functional kleptoplasts in the absence of the original algal nucleus and the limited number of proteins encoded by the chloroplast genome. This review updates the state-of-the-art on kleptoplast photophysiology, focusing on the comparative analysis of the responses to light of the chloroplasts when in their original, macroalgal cells, and when sequestered in animal cells and functioning as kleptoplasts. It covers fundamental but ecologically relevant aspects of kleptoplast light responses, such as the occurrence of photoacclimation in hospite, operation of photoprotective processes and susceptibility to photoinhibition. Emphasis is given to host-mediated processes unique to kleptoplastic associations, reviewing current hypotheses on behavioural photoprotection and host-mediated enhancement of photosynthetic performance, and identifying current gaps in sacoglossan kleptoplast photophysiology research.  相似文献   

2.
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.  相似文献   

3.
Some sacoglossan sea slugs have become famous for their unique capability to extract and incorporate functional chloroplasts from algal food organisms (mainly Ulvophyceae) into their gut cells. The functional incorporation of the so-called kleptoplasts allows the slugs to rely on photosynthetic products for weeks to months, enabling them to survive long periods of food shortage over most of their life-span. The algal food spectrum providing kleptoplasts as temporary, non-inherited endosymbionts appears to vary among sacoglossan slugs, but detailed knowledge is sketchy or unavailable. Accurate identification of algal donor species, which provide the chloroplasts for long-term retention is of primary importance to elucidate the biochemical mechanisms allowing long-term functionality of the captured chloroplast in the foreign animal cell environment. Whereas some sacoglossans forage on a variety of algal species, (e.g. Elysia crispata and E. viridis) others are more selective. Hence, characterizing the range of functional sacoglossan-chloroplast associations in nature is a prerequisite to understand the basis of this enigmatic endosymbiosis. Here, we present a suitable chloroplast gene (tufA) as a marker, which allows identification of the respective algal kleptoplast donor taxa by analysing DNA from whole animals. This novel approach allows identification of donor algae on genus or even species level, thus providing evidence for the taxonomic range of food organisms. We report molecular evidence that chloroplasts from different algal sources are simultaneously incorporated in some species of Elysia. NeigborNet analyses for species assignments are preferred over tree reconstruction methods because the former allow more reliable statements on species identification via barcoding, or rather visualize alternative allocations not to be seen in the latter.  相似文献   

4.
Long-term kleptoplasty, the capability to retain functional stolen chloroplasts (kleptoplasts) for several weeks to months, has been shown in a handful of Sacoglossa sea slugs. One of these sea slugs is Elysia timida, endemic to the Mediterranean, which retains functional chloroplasts of the macroalga Acetabularia acetabulum. To understand how light modulates the lipidome of E. timida, sea slug specimens were subjected to two different 4-week light treatments: regular light and quasi-dark conditions. Lipidomic analyses were performed by HILIC-HR-ESI-MS and MS/MS. Quasi-dark conditions caused a reduction in the amount of essential lipids for photosynthetic membranes, such as glycolipids, indicating high level of kleptoplast degradation under sub-optimal light conditions. However, maximum photosynthetic capacities (Fv/Fm) were identical in both light treatments (≈0.75), showing similar kleptoplast functionality and suggesting that older kleptoplasts were targeted for degradation. Although more stable, the phospholipidome showed differences between light treatments: the amount of certain lipid species of phosphatidylethanolamine (PE), phosphatidylinositol (PI), and phosphatidylglycerol (PG) decreased under quasi-dark conditions, while other lipid species of phosphatidylcholine (PC), PE and lyso-PE (LPE) increased. Quasi-dark conditions promoted a decrease in the relative abundance of polyunsaturated fatty acids. These results suggest a light-driven remodelling of the lipidome according to the functions of the different lipids and highlight the plasticity of polar lipids in the photosynthetic sea slug E. timida.  相似文献   

5.
Several sacoglossan sea slugs (Plakobranchoidea) feed upon plastids of large unicellular algae. Four species—called long-term retention (LtR) species—are known to sequester ingested plastids within specialized cells of the digestive gland. There, the stolen plastids (kleptoplasts) remain photosynthetically active for several months, during which time LtR species can survive without additional food uptake. Kleptoplast longevity has long been puzzling, because the slugs do not sequester algal nuclei that could support photosystem maintenance. It is widely assumed that the slugs survive starvation by means of kleptoplast photosynthesis, yet direct evidence to support that view is lacking. We show that two LtR plakobranchids, Elysia timida and Plakobranchus ocellatus, incorporate 14CO2 into acid-stable products 60- and 64-fold more rapidly in the light than in the dark, respectively. Despite this light-dependent CO2 fixation ability, light is, surprisingly, not essential for the slugs to survive starvation. LtR animals survived several months of starvation (i) in complete darkness and (ii) in the light in the presence of the photosynthesis inhibitor monolinuron, all while not losing weight faster than the control animals. Contrary to current views, sacoglossan kleptoplasts seem to be slowly digested food reserves, not a source of solar power.  相似文献   

6.

Background

Among metazoans, retention of functional diet-derived chloroplasts (kleptoplasty) is known only from the sea slug taxon Sacoglossa (Gastropoda: Opisthobranchia). Intracellular maintenance of plastids in the slug's digestive epithelium has long attracted interest given its implications for understanding the evolution of endosymbiosis. However, photosynthetic ability varies widely among sacoglossans; some species have no plastid retention while others survive for months solely on photosynthesis. We present a molecular phylogenetic hypothesis for the Sacoglossa and a survey of kleptoplasty from representatives of all major clades. We sought to quantify variation in photosynthetic ability among lineages, identify phylogenetic origins of plastid retention, and assess whether kleptoplasty was a key character in the radiation of the Sacoglossa.

Results

Three levels of photosynthetic activity were detected: (1) no functional retention; (2) short-term retention lasting about one week; and (3) long-term retention for over a month. Phylogenetic analysis of one nuclear and two mitochondrial loci revealed reciprocal monophyly of the shelled Oxynoacea and shell-less Plakobranchacea, the latter comprising a monophyletic Plakobranchoidea and paraphyletic Limapontioidea. Only species in the Plakobranchoidea expressed short- or long-term kleptoplasty, most belonging to a speciose clade of slugs bearing parapodia (lateral flaps covering the dorsum). Bayesian ancestral character state reconstructions indicated that functional short-term retention arose once in the last common ancestor of Plakobranchoidea, and independently evolved into long-term retention in four derived species.

Conclusion

We propose a sequential progression from short- to long-term kleptoplasty, with different adaptations involved in each step. Short-term kleptoplasty likely arose as a deficiency in plastid digestion, yielding additional energy via the release of fixed carbon. Functional short-term retention was an apomorphy of the Plakobranchoidea, but the subsequent evolution of parapodia enabled slugs to protect kleptoplasts against high irradiance and further prolong plastid survival. We conclude that functional short-term retention was necessary but not sufficient for an adaptive radiation in the Plakobranchoidea, especially in the genus Elysia which comprises a third of all sacoglossan species. The adaptations necessary for long-term chloroplast survival arose independently in species feeding on different algal hosts, providing a valuable study system for examining the parallel evolution of this unique trophic strategy.  相似文献   

7.
Factors determining the degree of dietary generalism versus specialism are central in ecology. Species that are generalists at the population level may in fact be composed of specialized individuals. The optimal diet theory assumes that individuals choose diets that maximize fitness, and individual specialization may occur if individuals'' ability to locate, recognize, and handle different food types differ. We investigate if individuals of the marine herbivorous slug Elysia viridis, which co-occur at different densities on several green macroalgal species in the field, are specialized to different algal hosts. Individual slugs were collected from three original algal host species (Cladophora sericea, Cladophora rupestris and Codium fragile) in the field, and short-term habitat choice and consumption, as well as long-term growth (proxy for fitness), on four algal diet species (the original algal host species and Chaetomorpha melagonium) were studied in laboratory experiments. Nutritional (protein, nitrogen, and carbon content) and morphological (dry weight, and cell/utricle volume) algal traits were also measured to investigate if they correlated with the growth value of the different algal diets. E. viridis individuals tended to choose and consume algal species that were similar to their original algal host. Long-term growth of E. viridis, however, was mostly independent of original algal host, as all individuals reached a larger size on the non-host C. melagonium. E. viridis growth was positively correlated to algal cell/utricle volume but not to any of the other measured algal traits. Because E. viridis feeds by piercing individual algal cells, the results indicate that slugs may receive more cytoplasm, and thus more energy per unit time, on algal species with large cells/utricles. We conclude that E. viridis individuals are specialized on different hosts, but host choice in natural E. viridis populations is not determined by the energetic value of seaweed diets as predicted by the ODT.  相似文献   

8.
The phenomenon of the uptake, intracellular sequestration, and subsequent usage of algal chloroplasts by the digestive cells of many species of sacoglossan sea slugs, currently called kleptoplasty, has been of considerable interest since its discovery in the 1960s. While a large body of literature reported that captured chloroplasts were photosynthetically active inside slug cells and that plastid longevity in some species might be the result of the horizontal transfer of functional algal nuclear genes into the slug genome, a few recent studies have called the older results into question. Here, we have reviewed the literature and showed that while kleptoplasty occurs in many slug species and almost all derive benefit from kleptoplast photosynthesis, the slug adaptations to maintain the chloroplasts differ from species to species. These adaptations range from behavioral to molecular, including gene transfer, in a variety of combinations.  相似文献   

9.
The kleptoplastic sacoglossan Elysia chlorotica shares a requisite, intracellular symbiosis with the plastids (= chloroplasts) of the Xanthophyte alga Vaucheria litorea. Although wild specimens have been used to address a range of biological questions, no studies have thoroughly characterized animal development during the initial establishment of the symbiosis under controlled laboratory conditions. Laboratory culture conditions were modified and the time required for successful metamorphosis was reduced by 40 % relative to previous work. Plastids were not initially stable within the host; “permanent kleptoplasty” was obtained only after ≥7 days of feeding on V. litorea. Feeding for shorter time periods resulted in the loss of plastids and abnormal development; this phase was characterized as “transient kleptoplasty”. Individuals in the transient state exhibited a significantly greater decrease in length compared to animals with permanent kleptoplasts after the same starvation period. To test the effect of food availability after obtaining permanent kleptoplasty, animals were subjected to various dietary regimes followed by a recovery period of constant feeding. Thirty percent of animals survived prolonged starvation (>4 weeks) after only the initial week of feeding required to establish permanent kleptoplasty. All treatments showed rapid growth when re-exposed to Vaucheria. Thus, during initial development E. chlorotica experiences enhanced fitness when Vaucheria is available for consumption. However, the animal rapidly establishes permanent kleptoplasty, which bestows flexible food requirements and resistance to food limitation, a likely advantage for E. chlorotica in salt marsh environments where Vaucheria sp. abundance is sporadic.  相似文献   

10.
The relationship of phenotypic morphological and behaviouralvariation was investigated for the ascoglossan (=sacoglossan)opisthobranch Placida dendritica. Morphological attributes weredocumented for individual slugs collected from three algal hostspecies along the central Oregon coast, USA, the green algaeCodium setchellii, C. fragile, and Bryopsis corticulans. Becauseindividuals on B. corticulans generally were substantially largerthan conspecifics on Codium spp., the species appeared polymorphic.Comparably sized slugs from different host genera also differedsignificantly in morphology: individuals from Codium spp. hadmore numerous, shorter cerata on wider bodies than did conspecificsfrom B. corticulans. Principal components analysis indicatedthat despite considerable overlap of morphological characters,ceratal shape features were diagnostic of algal host. When slugscollected from C. fragile were maintained on C. fragile andB. corticulans for 4 days in the laboratory, the size and shapeof slugs fed different diets diverged, and changes were consistentwith field data. Thus, phenotype was labile and changed as aresult of modified diet. Although a variety of molluscs exhibitdietary induction of morphology, a general awareness of thephenomenon has only recently begun to emerge, despite its importantecological and taxonomic implications. (Received 5 February 1996; accepted 2 July 1996)  相似文献   

11.
Solar-powered sea slugs (Sacoglossa: Gastropoda) have long captured the attention of laymen and scientists alike due to their remarkable ability to steal functional chloroplasts from their algal food, enslaving them to withstand long starvation periods. Recently, a wealth of data has shed insight into this remarkable relationship; however, the cellular mechanisms governing this process are still completely unknown. This study explores these mechanisms, providing insight into the chloroplast retention and delayed digestion, occurring within the slug’s digestive gland. We examine the relationships between functional chloroplast and lysosome abundances during starvation, in live material, for the long-term retaining species Elysia timida, the ambiguous long/short-term retaining Elysia viridis, and the short-term retaining Thuridilla hopei, to elucidate digestive differences that contribute to the development of functional kleptoplasty. Functional chloroplast and lysosome abundance are measured using chlorophyll a autofluorescence and the pH-dependent stain acridine orange. In each species, the number of chloroplasts and lysosomes is indirectly proportional, with the plastid density decreasing when starvation begins. We also present a new FIJI/Image J Plugin, the 3D—Accounting and Measuring Plugin, 3D-AMP, which enables the reliable analysis of large image sets.  相似文献   

12.
The capacity of sea slugs (sacoglossans) for retaining chloroplasts from food algae provides important insights into endosymbiotic relationships and kleptoplasty. A sea slug species was captured accidentally in the Yellow Sea and identified as Placida sp. YS001 based on phylogenetic analyses of the COX1 and 16S gene sequence. Its life cycle was recorded using microscope. Photosynthetic analysis by pulse amplitude modulated fluorometry during starvation revealed shortterm functional kleptoplasty. An ultrastructural comparison of the slug and alga showed that a change in the chloroplast structure and the phagosome might correspond to short-term endosymbiosis. The horizontally transferred genes, psbO and lectin, were not cloned in the adults or eggs. This study demonstrates the morphological adaptation that occurs during short-term endosymbiotic relationships and provides fresh insights.  相似文献   

13.
The sea slug Plakobranchus ocellatus (Sacoglossa, Gastropoda) retains photosynthetically active chloroplasts from ingested algae (functional kleptoplasts) in the epithelial cells of its digestive gland for up to 10 months. While its feeding behavior has not been observed in natural habitats, two hypotheses have been proposed: 1) adult P. ocellatus uses kleptoplasts to obtain photosynthates and nutritionally behaves as a photoautotroph without replenishing the kleptoplasts; or 2) it behaves as a mixotroph (photoautotroph and herbivorous consumer) and replenishes kleptoplasts continually or periodically. To address the question of which hypothesis is more likely, we examined the source algae for kleptoplasts and temporal changes in kleptoplast composition and nutritional contribution. By characterizing the temporal diversity of P. ocellatus kleptoplasts using rbcL sequences, we found that P. ocellatus harvests kleptoplasts from at least 8 different siphonous green algal species, that kleptoplasts from more than one species are present in each individual sea slug, and that the kleptoplast composition differs temporally. These results suggest that wild P. ocellatus often feed on multiple species of siphonous algae from which they continually obtain fresh chloroplasts. By estimating the trophic position of wild and starved P. ocellatus using the stable nitrogen isotopic composition of amino acids, we showed that despite the abundance of kleptoplasts, their photosynthates do not contribute greatly to the nutrition of wild P. ocellatus, but that kleptoplast photosynthates form a significant source of nutrition for starved sea slugs. The herbivorous nature of wild P. ocellatus is consistent with insights from molecular analyses indicating that kleptoplasts are frequently replenished from ingested algae, leading to the conclusion that natural populations of P. ocellatus do not rely on photosynthesis but mainly on the digestion of ingested algae.  相似文献   

14.
Several species of kleptoplastic, sacoglossan sea slug photosynthesize using chloroplasts sequestered inside their digestive cells from algal food sources. However, sequestered chloroplasts alone are not sufficient for months-long, continuous photosynthesis and maintenance of the chloroplasts in absence of the algal nucleus. Some type of plastid maintenance mechanism must be present to help sustain photosynthetic activity in the long term kleptoplastic species, such as Elysia clarki. We demonstrate that E. clarki starved for 2 weeks are able to synthesize chlorophylls, but that slugs starved for 14 weeks no longer synthesize chlorophyll. The subsidence of chlorophyll synthesis is coincident with the cessation of photosynthesis by the starved slugs, but it is not yet known if the cessation of pigment synthesis is the cause or some other aspect of plastid degradation produces a loss of synthetic ability.  相似文献   

15.
Sacoglossans are characterized by the ability to sequester functional chloroplasts from their algal diet through a process called kleptoplasty, enabling them to photosynthesize. The bacterial diversity associated with sacoglossans is not well understood. In this study, we coupled traditional cultivation-based methods with 454 pyrosequencing to examine the bacterial communities of the chemically defended Hawaiian sacoglossan Elysia rufescens and its secreted mucus. E. rufescens contains a defense molecule, kahalalide F, that is possibly of bacterial origin and is of interest because of its antifungal and anticancer properties. Our results showed that there is a diverse bacterial assemblage associated with E. rufescens and its mucus, with secreted mucus harboring higher bacterial richness than entire-E. rufescens samples. The most-abundant bacterial groups affiliated with E. rufescens and its mucus are Mycoplasma spp. and Vibrio spp., respectively. Our analyses revealed that the Vibrio spp. that were highly represented in the cultivable assemblage were also abundant in the culture-independent community. Epifluorescence microscopy and matrix-assisted laser desorption–ionization mass spectrometry (MALDI-MS) were utilized to detect the chemical defense molecule kahalalide F on a longitudinal section of the sacoglossan.  相似文献   

16.
The importance of photosynthetic products derived from kleptoplasts in several sacoglossan species is being investigated in different fields, such as chemistry, biomolecular genetics and ecology. This study analyzes the effect of kleptoplasts on the survival rates of Elysia timida by evaluating the development of chlorophyll concentration, total length and survival rates of starved E. timida specimens kept in the light and in the dark. Although chlorophyll concentration values were similar in both cases, after 28 days specimens kept in the dark showed a greater size decrease and a lower survival rate (up to 30% lower) than those kept in the light. It is evident that kleptoplasts provide the mollusc with extra energy at the primary metabolism level to compensate for a shortage in food.  相似文献   

17.
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 animals <5 dpm that had not yet achieved permanent kleptoplasty. Animals allowed to feed on algal prey (Vaucheria litorea C. Agardh) for 7 d or greater retained stable plastids resistant to cellular breakdown. Lipid analysis of algal and animal samples supports that these accumulating LDs may be of plastid origin, as the often algal-derived 20∶5 eicosapentaenoic acid was found in high abundance in the animal tissue. Subsequent culturing of animals in dark conditions revealed a reduced ability to establish permanent kleptoplasty in the absence of photosynthetic processes, coupled with increased mortality. Together, these data support an important role of photosynthetic lipid production in establishing and stabilizing this unique animal kleptoplasty.  相似文献   

18.
The sacoglossan sea slug, Plakobranchus ocellatus, is a so-called long-term retention form that incorporates chloroplasts for several months and thus is able to starve while maintaining photosynthetic activity. Little is known regarding the taxonomy and food sources of this sacoglossan, but it is suggested that P. ocellatus is a species complex and feeds on a broad variety of Ulvophyceae. In particular, we analysed specimens from the Philippines and starved them under various light conditions (high light, low light and darkness) and identified the species of algal food sources depending on starvation time and light treatment by means of DNA-barcoding using for the first time the combination of two algal chloroplast markers, rbcL and tufA. Comparison of available CO1 and 16S sequences of specimens from various localities indicate a species complex with likely four distinct clades, but food analyses do not indicate an ecological separation of the investigated clades into differing foraging strategies. The combined results from both algal markers suggest that, in general, P. ocellatus has a broad food spectrum, including members of the genera Halimeda, Caulerpa, Udotea, Acetabularia and further unidentified algae, with an emphasis on H. macroloba. Independent of the duration of starvation and light exposure, this algal species and a further unidentified Halimeda species seem to be the main food source of P. ocellatus from the Philippines. It is shown here that at least two (or possibly three) barcode markers are required to cover the entire food spectrum in future analyses of Sacoglossa.  相似文献   

19.
Preferential consumption of algal reproductive tissues has been predicted to potentially reduce algal fitness by reduction of reproductive output. This study shows that the amphipod Hyale media (Dana) has a marked trophic preference for mature cystocarpic tissues of Iridaea laminarioides Bory. However, during the feeding process the amphipod tears the cystocarps releasing large numbers of spores into the water column. Germination and growth rate experiments indicate that grazer-mediated release does not affect further spore development. Field populations of I. laminarioides might have unopened cystocarps even in senescent, decaying fronds, while the total number of open cystocarps in mature and senescent fronds increases at higher amphipod density sites, suggesting a facilitation mechanism. Laboratory observations indicate spores can stick to the legs and body sides of the amphipods while a fraction of the ingested spores survives passage through the amphipod digestive tract. Thus, the amphipod seems ecologically important not only as a grazer but also as spore releaser and disperser.  相似文献   

20.
Elysia viridis (Montagu) occurs naturally in populations feedingon the fleshy, siphonalean green alga Codium or on the coarse,filamentous green alga Chaetomorpha. Only about half of theE. viridis transferred from Codium to Chaetomorpha in the laboratorywere able to learn to feed on this alga. Handling time decreasedsignificantly during the learning-period. All E. viridis transferredfrom Chaetomorpha to Codium in the laboratory were able to learnto feed on the latter alga. Handling time also decreased withexperience in these animals. Ingestive conditioning occurredin animals transferred from Chaetomorpha to Codium. These animalshad to go through a learning-period again when they were offeredChaetomorpha after 6–9 weeks with Codium Ingestive conditioningwas also evident from preference experiments; animals preferredthe food they had been kept on prior to the experiments. Thesefindings are discussed in relation to optimal diet theory. (Received 14 December 1987; accepted 22 March 1988)  相似文献   

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