Mollusc/algal chloroplast symbiosis: how can isolated chloroplasts continue to function for months in the cytosol of a sea slug in the absence of an algal nucleus?

Rumpho, Mary E.; Summer, Elizabeth J.; Green, Brian J.; Fox, Theodore C.; Manhart, James R.

doi:10.1078/0944-2006-00036

Cited by 61 publications

(65 citation statements)

References 41 publications

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“…Thus, via succinate, 14 CO 2 can be incorporated into animal tissue, but in a light-independent manner. Furthermore, the fixation rates reported so far vary substantially between different species studied [23,32,33,[43][44][45]. We investigated the ability of E. timida bearing Acetabularia plastids to fix 14 CO 2 in the absence and presence of light.…”

Section: Resultsmentioning

confidence: 99%

“…The PCR amplification products for PsbO obtained from E. chlorotica were identical in sequence to those from Vaucheria, including a canonical bipartite targeting signal [21,22] that directs the PsbO precursor across the four membranes that surround the plastid in Vaucheria. However, the Vaucheria plastids that are sequestered in E. chlorotica are only surrounded by two membranes; the outer two are removed during sequestration [23]. As a consequence, were the E. chlorotica PsbO precursor protein [20] really expressed, the gene product would enter the secretory pathway, and thus be excreted from the cell because of its intact and highly conserved signal peptide, rather than being targeted to the remaining inner two membranes of the sequestered Vaucheria plastid [8].…”

Section: Introductionmentioning

confidence: 99%

“…A number of other studies also reported the incorporation of 14 C from 14 CO 2 in plakobranchids that sequester plastids [30][31][32][33], but animals can also incorporate CO 2 via carboxylation reactions. The second line of evidence for plakobranchids being photosynthetic comes from the observation that once the plastids have been incorporated into the digestive gland, LtR species can survive for months in the absence of additional food [7,10,23,24,34,35]. Such plakobranchids are said to be 'starved' and are typically cultivated in the light [8,9].…”

Section: Introductionmentioning

confidence: 99%

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Plastid-bearing sea slugs fix CO₂in the light but do not require photosynthesis to survive

et al. 2014

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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 14 CO 2 into acid-stable products 60-and 64-fold more rapidly in the light than in the dark, respectively. Despite this light-dependent CO 2 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.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Plastid-bearing sea slugs fix CO₂in the light but do not require photosynthesis to survive

et al. 2014

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“…The plastids do not undergo division in the sea slug and are sequestered intracellularly in cells lining the finely divided digestive diverticula. The plastids continue to carry out photosynthesis, providing the sea slug with energy and carbon during its approximately 10-month life span (27,28). Long-term plastid activity continues despite the absence of algal nuclei (27,29), and hence a source of nuclear-encoded plastid-targeted proteins.…”

mentioning

confidence: 99%

“…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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241

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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How to Lose the Plasmalemma? Lessons From Ciliates, Dinoflagellates and Euglenids

Bodył

2017

BioEssays

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Mollusc/algal chloroplast symbiosis: how can isolated chloroplasts continue to function for months in the cytosol of a sea slug in the absence of an algal nucleus?

Cited by 61 publications

References 41 publications

Plastid-bearing sea slugs fix CO₂in the light but do not require photosynthesis to survive

Plastid-bearing sea slugs fix CO₂in the light but do not require photosynthesis to survive

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

How to Lose the Plasmalemma? Lessons From Ciliates, Dinoflagellates and Euglenids

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Mollusc/algal chloroplast symbiosis: how can isolated chloroplasts continue to function for months in the cytosol of a sea slug in the absence of an algal nucleus?

Cited by 61 publications

References 41 publications

Plastid-bearing sea slugs fix CO2in the light but do not require photosynthesis to survive

Plastid-bearing sea slugs fix CO2in the light but do not require photosynthesis to survive

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

How to Lose the Plasmalemma? Lessons From Ciliates, Dinoflagellates and Euglenids

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Plastid-bearing sea slugs fix CO₂in the light but do not require photosynthesis to survive

Plastid-bearing sea slugs fix CO₂in the light but do not require photosynthesis to survive