The Kleptoplast

Rumpho, Mary E.; Dastoor, Farahad; Manhart, James R.; Lee, Jung-Ho

doi:10.1007/1-4020-4061-x_23

Cited by 7 publications

(11 citation statements)

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“…Because kleptoplasts have not been observed to divide [2], [17], these changes must result from the replacement of kleptoplasts with newly obtained chloroplasts by feeding, different spans of longevity among kleptoplasts derived from various source algae, and/or differential kleptoplast DNA replication (multimerization) rates [47], [48] due to those source algae.…”

Section: Discussionmentioning

confidence: 99%

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Algivore or Phototroph? Plakobranchus ocellatus (Gastropoda) Continuously Acquires Kleptoplasts and Nutrition from Multiple Algal Species in Nature

et al. 2012

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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.

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Section: Discussionmentioning

confidence: 99%

“…Since the discovery of “chloroplast retention” in Elysia atroviridis by Kawaguti & Yamasu [1], it has been widely accepted that many species of sacoglossan sea slugs (Sacoglossa, Gastropoda, Mollusca) retain chloroplasts of ingested algae in digestive gland cells [2]. A sequestered chloroplast is called a “kleptoplast” [3].…”

Section: Introductionmentioning

confidence: 99%

Algivore or Phototroph? Plakobranchus ocellatus (Gastropoda) Continuously Acquires Kleptoplasts and Nutrition from Multiple Algal Species in Nature

et al. 2012

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“…This is a large species by sacoglossan standards (up to five cm long), and the subject of prior studies on chloroplast retention [[71], as P. ianthobapsus , [72], as P. ianthobapsus , [27,45]]. E. chlorotica , a species best known for its long-term retention, was not available for PAM measurements but its photosynthetic ability is well documented [46,73-77]. …”

Section: Discussionmentioning

confidence: 99%

“…and T. hopei lost photosynthetic activity within a few days (Figures 1 and 2). The record for chloroplast retention is 14 months for E. chlorotica [46]. …”

Section: Introductionmentioning

confidence: 99%

Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life

et al. 2009

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BackgroundAmong 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.ResultsThree 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.ConclusionWe 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.

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“…This emerald green sea slug owes its coloring and photosynthetic ability to plastids acquired during herbivorous feeding (24)(25)(26)(27)(28)(29). The plastids do not undergo division in the sea slug and are sequestered intracellularly in cells lining the finely divided digestive diverticula.…”

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confidence: 99%

Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica

Rumpho

Worful²,

Lee³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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238

169

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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.symbiosis ͉ Vaucheria litorea ͉ evolution ͉ plastid ͉ stramenopile

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The Kleptoplast

Cited by 7 publications

References 0 publications

Algivore or Phototroph? Plakobranchus ocellatus (Gastropoda) Continuously Acquires Kleptoplasts and Nutrition from Multiple Algal Species in Nature

Algivore or Phototroph? Plakobranchus ocellatus (Gastropoda) Continuously Acquires Kleptoplasts and Nutrition from Multiple Algal Species in Nature

Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life

Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica

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