Chloroplast symbiosis

Here is a list of published work on animals, mainly sacoglossan opisthobranchs, which have evolved symbiotic relationships with chloroplasts they have removed from plant tissue. The papers cover all aspects of the symbiosis, from morphological changes in the animal to physiological chnages in the plastid. Any additional references are welcome.

See Solar-powered Sea Slugs.

• Brandley, B (1984): Aspects of the ecology and physiology of Elysia cf. furvacauda (Mollusca: Sacoglossa). Bull. Mar. Sci. 34(2), 207-219.
• Clark, KB; Busacca, M (1978): Feeding specificity and chloroplast retention in four tropical ascoglossa, with a discussion of the extent of chloroplast symbiosis and the evolution of the order. J. Moll. Stud. 44, 272-282,Figs1-3.
• Clark, KB; Jensen, KR; Stirts, HM; Fermin, C (1981): Chloroplast symbiosis in a non-elysiid mollusc, Costasiella lilianae Marcus (Hermaeidae: Ascoglossa (=Sacoglossa)): Effects of temperature, light intensity, and starvation on carbon fixation rate. Biol. Bull. 160(1), 43-54.
• Clark, K.B., Jensen, K.R. & Stirts, H.M. (1990) Survey for functional kleptoplasty among west Atlantic Ascoglossa (=Sacoglossa) (Mollusca: Opisthobranchia). The Veliger, 33: 339-345.
• Clark, K.B. 1992. Plant-like animals and animal-like plants: symbiotic coevolution of ascoglossan (=sacoglossan) molluscs, their algal prey, and algal plastids. pp. 515-530 [In] (W. Reisser, ed.) Algae and symbioses: plants, animals, fungi, viruses, interactions explored. Biopress Ltd., Bristol, U.K.
• Graves, DA; Gibson, MA; Bleakney, JS (1979): The digestive diverticula of Alderia modesta and Elysia chlorotica (Opisthobranchia: Sacoglossa). The Veliger 21(4), 415-422. (Figs 1-15)
• Green, B.J., Li, W-Y., Manhart, J.R., Fox, T.C., Summer, E.J., Kennedy, R.A., Pierce, S.K. & Rumpho, M.E. (2000) Mollusc-Algal Chloroplast Endosymbiosis. Photosynthesis, Thylakoid Protein Maintenance, and Chloroplast Gene Expression Continue for Many Months in the Absence of the Algal Nucleus. Plant Physiology, 124: 331-342.
• Hanten, J.J. and S.K. Pierce. (2001) Synthesis of several light-harvesting complex I polypeptides is blocked by cycloheximide in symbiotic chloroplasts in the sea slug, Elysia chlorotica (Gould): A case for horizontal gene transfer between alga and animal? Biological Bulletin, 201: 33-44.
• Hinde, R; Smith, DC (1974): `Chloroplast symbiosis' and the extent to which it occurs in Sacoglossa (Gastropoda: Mollusca). Biol. J. Linn. Soc. 6(4), 349-356.
• Hinde, R; Smith, DC (1975): The role of photosynthesis in the nutrition of the mollusc Elysia viridis. Biol. J. Linn. Soc. 7, 161-171.
• Ireland, C; Scheuer, PJ (1979): Photosynthetic marine mollusks: In vivo Carbon 14 incorporation into metabolites of the sacoglossan Placobranchus ocellatus. Science 205(4409), 922-923.
• Jensen, KR (1985): Annotated checklist of Hong Kong Ascoglossa (Mollusca: Opisthobranchia), with descriptions of four new species. In: Proceedings of the 2nd International Workshop on the Malacofauna of Hong Kong and Southern China, Hong Kong, 1983. (Eds: Morton,B; Dudgeon,D) Hong Kong University Press, Hong Kong, 77-107.
• Kawaguti, S; Yamasu, T (1965): Electron microscopy on the symbiosis between an elysioid gastropod and chloroplasts of a green alga. Biol. J. Okayama Univ. 11(3-4), 57-65.
• Marin, A; Ros, JD (1988): The Sacoglossa (Mollusca, Opisthobranchia) of the South East Iberian peninsula. A Catalogue of species and presence of algal chloroplasts in them. Iberus 8(1), 25-49.
• Marin, A; Ros, JD (1992): Dynamics of a peculiar plant-herbivore relationship: the photosynthetic ascoglossan Elysia timida and the chlorophycean Acetabularia acetabulum. Marine Biology 112, 677-682,Figs1-10.
• Monselise, EB; Rahat, M (1980): Photobiology of Elysia timida (Mollusca: Opisthobranchia): observations in the sea. Isr. J. Zool. 29(1-3), 125-128.
• Mujer CV, Andrews DL, Manhart JR, Pierce SK, Rumpho ME (1996) Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proc Natl Acad Sci U S A, 93(22):12333-8
• Pierce S, Biron R, Rumpho M. (1996) Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J Exp Biol, 199(10):2323-30
• Pierce, S. K., Maugel, T. K., Rumpho, M. E., Hanten, J. J., Mondy, W. L. (1999). Annual viral expression in a sea slug population: Life cycle control and symbiotic chloroplast maintenance. Biological Bulletin, 196: 197: 1-6.
• Pierce, S.K., Massey, S.E., Hanten, J.J. &. Curtis, N.E. (2003). Horizontal Transfer of Functional Nuclear Genes Between Multicellular Organisms. Biological Bulletin, 204: 237-240.
• Rahat, M; Ben-Izhak Monselise, E (1979): Photobiology of the chloroplast hosting mollusc Elysia timida (Opisthobranchia). J. Exp. Biol. 79, 225-233.
• Roller, RA; Bianchi, TS (1995): HPLC analysis of chloroplast pigments from the marine ascoglossan Tridachia crispata (Morch, 1863) (Mollusca: Opisthobranchia). American Malacological Bulletin 11(2), 139-143.
• Ros, J; Rodriguez, J (1985): La simbiosis algal en Elysia timida Risso 1818. Primeros resultados. Anales de Biologia 4(Biologia Ambiental, 1), 37-47.
• Ros, J (1978): Distribucion en l'espai i en el temps dels opistobranquis Iberics, amb especial referencia als del litoral Catal…. Butllet¡ de la Institucio Catalana d'Historia Natural 42(Sec. Zool., 2), 23-32.
• Rumpho, M.E., Summer, E.J. & Manhart, J.R. (2000)
Solar-Powered Sea Slugs. Mollusc/Algal Chloroplast Symbiosis. Plant Physiology, 123: 29-38.
• Taylor, DL (1967): The occurrence and significance of endosymbiotic chloroplasts in the digestive glands of herbivorous opisthobranchs. Journal of Phycology, 3, 234-235.
• Taylor, DL (1971): Symbiosis between the chloroplasts of Griffithsia flosculosa and Hermaea bifida. Publicaziones della Stazione Zoologia Napoli 39, 116-120.
• Trench, ME; Trench, RK; Muscatine, L (1970): Utilization of photosynthetic products of symbiotic chloroplasts in mucus synthesis by Placobranchus ianthobapsus (Gould), Opisthobranchia, Sacoglossa. Comp. Biochem. Physiol. 37, 113-117.
• Trench, RK; Smith, DC (1970): Synthesis of pigment in symbiotic chloroplasts. Nature 227, 196-197.
• Trench, RK; Boyle, JE; Smith, DC (1973): The association between chloroplasts of Codium fragile and the mollusc Elysia viridis. I. Characteristics of isolated Codium chloroplasts. Proceedings of the Royal Society, London B, 184, 51-61.
• Trench, RK; Boyle, JE; Smith, DC (1973): The association between chloroplasts of Codium fragile and the mollusc Elysia viridis. II. Chloroplast ultrastructure and photosynthetic carbon fixation in E. viridis. Proceedings of the Royal Society, London B, 184, 63-81.
• Trench, RK; Boyle, JE; Smith, DC (1974): The association between chloroplasts of Codium fragile and the mollusc Elysia viridis. III. Movement of photosynthetically fixed Carbon 14 in tissues of intact living E. viridis and in Tridachia crispata. Proceedings of the Royal Society, London B, 185, 453-464.
• Waugh, GR; Clark, KB (1986): Seasonal and geographic variation in chlorophyll level of Elysia tuca (Ascoglossa: Opisthobranchia). Marine Biology 92, 483-487.
• Weaver, S; Clark, KB (1981): Light intensity and color preferences of five ascoglossan (=sacoglossan) Molluscs (Gastropoda: Opisthobranchia): a comparision of chloroplast-symbiotic and aposymbiotic species. Marine Behaviour and Physiology, 7, 297-306.
• Williams, S.I. & Walker, D.I. (1999) Mesoherbivore-macroalgal interactions: Feeding ecology of sacoglossan sea slugs (Mollusca, Opisthobranchia) and their effects on their food algae. Oceanography and Marine Biology Annual Review, 37: 87-128.
• Yonge, CM; Nicholas, HM (1940): Structure and function of the gut and symbiosis with zooxanthellae in Tridachia crispata (Oerst.) Bgh. Papers from Tortugas Laboratory 32(14 September), 289-301.

Authorship details
Rudman, W.B., 1998 (October 11) Chloroplast symbiosis . [In] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/find/chloropl

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Related messages

Re: Review of sacoglossan - plastid symbiosis

May 19, 2000
From: C.D. Trowbridge

Dear Bill,

I would like to add that there is another major review on ascoglossan/sacoglossan herbivores and kleptoplasty by Sue Williams and Di Walker (UWA) in 1999 in Oceanography and Marine Biology Annual Review, vol. 37.

I hope all slug workers are sending their publication info to Steve Long for inclusion in the Opisthobranch Newsletter and the searchable literature database. Steve's database is a wonderful resource, particularly as he has added keywords of all opisthobranchs mentioned in each paper.

Cordially, Cynthia

Hatfield Marine Science Center
Oregon State University

trowbric@ucs.orst.edu

Trowbridge, C.D., 2000 (May 19) Re: Review of sacoglossan - plastid symbiosis. [Message in] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/find/2409

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Re: Chloroplast symbiosis references

May 18, 2000
From: Kathe R. Jensen

Hi Bill,
I have the following additions to your list of references on chloroplast symbiosis:

Clark, K.B., Jensen, K.R. & Stirts, H.M. 1990. Survey for functional kleptoplasty among west Atlantic Ascoglossa (=Sacoglossa) (Mollusca: Opisthobranchia). Veliger 33: 339-345.

Clark, K.B. 1992. Plant-like animals and animal-like plants: symbiotic coevolution of ascoglossan (=sacoglossan) molluscs, their algal prey, and algal plastids. pp. 515-530 in (W. Reisser, ed.) Algae and symbioses: plants, animals, fungi, viruses, interactions explored. Biopress Ltd., Bristol, U.K.

Williams, S.I. & Walker, D.I. 1999. Mesoherbivore-macroalgal interactions: Feeding ecology of sacoglossan sea slugs (Mollusca, Opisthobranchia) and their effects on their food algae. Oceanography and Marine Biology Annual Review 37: 87-128.

Kathe R. Jensen

jensen@ait.ac.th

Jensen, K. R., 2000 (May 18) Re: Chloroplast symbiosis references. [Message in] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/find/2408

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Chloroplast retention in Elysia

August 25, 1999
From: Marc-André Selosse

Hello !

I found your question about Elysia. Please find here two references on the (very long) survival of plastids in Elysia chlorotica:

1. Pierce S, Biron R, Rumpho M. (1996)
Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J Exp Biol;199(Pt 10):2323-30

Endosymbiotic chloroplasts within the cells of the ascoglossan slug Elysia chlorotica synthesize a variety of proteins including the large subunit of
ribulose-1,5-bisphosphate-carboxylase oxygenase (RuBisCO) and the photosystem II protein D1. In addition, the effects of protein synthesis inhibitors suggest that some chloroplast-associated proteins are synthesized in the animal cytosol and subsequently translocated into the chloroplasts. Thus, the plastids not only synthesize proteins during this long-lived association, but the host cell seems to play a role in plastid protein turnover.

2. Mujer CV, Andrews DL, Manhart JR, Pierce SK, Rumpho ME (1996) Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proc Natl Acad Sci U S A, 93(22):12333-8

The marine slug Elysia chlorotica (Gould) forms an intracellular symbiosis with photosynthetically active chloroplasts from the chromophytic alga Vaucheria litorea (C. Agardh). This symbiotic association was characterized over a period of 8 months during which E. chlorotica was deprived of V. litorea but provided with light and CO2. The fine structure of the symbiotic chloroplasts remained intact in E. chlorotica even after 8 months of starvation as revealed by electron microscopy. Southern blot analysis of total DNA from E. chlorotica indicated that algal genes, i.e., rbcL, rbcS, psaB, psbA, and 16S rRNA are present in the animal. These genes are typically localized to the plastid genome in higher plants and algae except rbcS, which is nuclear-encoded in higher plants and green (chlorophyll a/b) algae. Our analysis suggests, however, that similar to the few other chromophytes (chlorophyll a/c) examined, rbcS is chloroplast encoded in V.litorea. Levels of psbA transcripts remained constant in E. chlorotica starved for 2 and 3 months and then gradually declined over the next 5 months corresponding with senescence of the animal in culture and in nature.
The RNA synthesis inhibitor 6-methylpurine reduced the accumulation of psbA transcripts confirming active transcription. In contrast to psbA, levels of 16S rRNA transcripts remained constant throughout the starvation period. The levels of the photosystem II proteins, D1 and CP43, were high at 2 and 4 months of starvation and remained constant at a lower steady-state level after 6 months. In contrast, D2 protein levels, although high at 2 and 4 months, were very low at all other periods of starvation. At 8 months, de novo synthesis of several thylakoid membrane-enriched proteins, including D1, still occurred. To our knowledge, these results represent the first molecular evidence for active transcription and translation of algal chloroplast genes in an animal host and are discussed in relation to the endosymbiotic theory of eukaryote origins.

Sincerely yours,

Marc-André

M.-A. SELOSSE
NANCY
FRANCE

ma.selosse@wanadoo.fr

Selosse, M., 1999 (Aug 25) Chloroplast retention in Elysia. [Message in] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/find/1244

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Chloroplast symbiosis references

March 9, 1999
From: Bill Rudman

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