Kleptoplasty

Kleptoplasty in Elysia chlorotica. The slug on the left sucks the sap from its food plant, Vaucheria, shcematized at top. Chloroplasts (red circles) are taken into the slug's cells at bottom, enabling the animal's cells to perform photosynthesis. From Rumpho et al., 2011, J. Exp. Biol. 214: 303.

Kleptoplasty in Elysia chlorotica. The slug on the left sucks the sap from its food plant, Vaucheria litorea., Chloroplasts (red circles) are taken from the algal cells at top into the slug’s cells at bottom, enabling the animal’s cells to perform photosynthesis. From Rumpho et al., 2011, J. Exp. Biol. 214: 303.

Based on the number of papers below and the number of articles that have appeared in the popular press, this aspect of Elysia biology gets the most attention.  When Elysia species feed on their host algae, they can retain the chloropasts, which are referred to as “kleptoplasts” after having been stolen from the plants.  Depending on the species of Elysia, these kelptoplasts can survive for many months in digestive diverticula that extend throughout the animals’ bodies.  Although the animals must still eat to survive, the kleptoplasts continue to perform photosynthesis in the animals’ bodies.

Scientific Literature

Baumgartner, F.A., Pavia, H., Toth, G.B. (2015) Acquired phototrophy through retention of functional chloroplasts increases growth efficiency of the sea slug Elysia viridis. PLoS ONE, 10 (4), art. no. e0120874 [F] [K] [Vi]

de Vries, J., Rauch, C., Christa, G., Gould, S.B. (2014) A sea slug’s guide to plastid symbiosis. Acta Soc Bot Pol 83(4):415–421 [K] [R]

Curtis, N.E., Middlebrooks, M.L., Schwartz, J.A., Pierce, S.K. (2015) Kleptoplastic sacoglossan species have very different capacities for plastid maintenance despite utilizing the same algal donors. Symbiosis, 65 (1), pp. 23-31 [F] [K] [Cl] [Pp]

Christa, G., Händeler, K., Kück, P., Vleugels, M., Franken, J., Karmeinski, D., Wägele, H. (2014) Phylogenetic evidence for multiple independent origins of functional kleptoplasty in Sacoglossa (Heterobranchia, Gastropoda). Organisms Diversity and Evolution, 15 (1), pp. 23-36 [K] [F] [Cl] [Pp] [Pt] [Zu]

Pelletreau, K.N., Weber, A.P.M., Weber, K.L., Rumpho, M.E. (2014) Lipid accumulation during the establishment of kleptoplasty in Elysia chlorotica. PLoS ONE, 9 (5), art. no. e97477. [K] [Cl]

Serôdio, J., Cruz, S., Cartaxana, P., Calado, R. (2014) Photophysiology of kleptoplasts: Photosynthetic use of light by chloroplasts living in animal cells. Philosophical Transactions of the Royal Society B: Biological Sciences, 369 (1640), 20130242. [K] [R]

Schwartz, J.A., Curtis, N.E., Pierce, S.K. (2014) FISH labeling reveals a horizontally transferred algal (vaucheria litorea) nuclear gene on a sea slug (elysia chlorotica) chromosome. Biological Bulletin, 227 (3), pp. 300-312. [HT] [K] [Ch]

de Vries, J., Crista, G., Gould, S.B. (2014) Plastid survival in the cytosol of animal cells.  Trends in Plant Science 1168 [K] [R]

Christa, G., Händeler, K., Schäberle, T.F., König, G.M., Wägele, H. (2014) Identification of sequestered chloroplasts in photosynthetic and non-photosynthetic sacoglossan sea slugs (Mollusca, Gastropoda) Frontiers in Zoology, 11 (1), art. no. 15. Abstract PDF [F] [K]

Schmitt, V., Händeler, K., Gunkel, S., Escande, M.-L., Menzel, D., Gould, S.B., Martin, W.F., Wägele, H. (2014) Chloroplast incorporation and long-term photosynthetic performance through the life cycle in laboratory cultures of Elysia timida (sacoglossa, heterobranchia). Frontiers in Zoology, 11 (1), art. no. 5, . Abstract PDF [AQ] [F] [K] [Ti]

Middlebrooks, M.L., Bell, S.S., Curtis, N.E., Pierce, S.K. (2014) Atypical plant-herbivore association of algal food and a kleptoplastic sea slug (Elysia clarki) revealed by DNA barcoding and field surveys. Marine Biology, 161 (6), pp. 1429-1440.  Abstract [F] [K] [Cl]

Akimoto, A., Hirano, Y.M., Sakai, A., Yusa, Y. (2014) Relative importance and interactive effects of photosynthesis and food in two solar-powered sea slugs. Marine Biology, 161 (5), pp. 1095-1102. Abstract [F] [K] [At] [Tr]

Christa, G., Zimorski, V., Woehle, C., Tielens, A.G.M., Wägele, H., Martin, W.F., Gould, S.B. (2013) Plastid-bearing sea slugs fix CO2 in the light but do not require photosynthesis to survive. Proceedings of the Royal Society B: Biological Sciences, 281 (1774), art. no. 20132493. Abstract [K] [Ti] [contains phylogenetic analysis of Plakobranchia]

Martin, R., Walther, P., Tomaschko, K.-H. (2013) Phagocytosis of algal chloroplasts by digestive gland cells in the photosynthesis-capable slug Elysia timida (Mollusca, Opisthobranchia, Sacoglossa). Zoomorphology, 132 (3), pp. 253-259. Abstract [K] [Ti]

Bhattacharya, D., Pelletreau, K.N., Price, D.C., Sarver, K.E., Rumpho, M.E.(2013) Genome analysis of Elysia chlorotica egg DNA provides no evidence for horizontal gene transfer into the germ line of this kleptoplastic mollusc Molecular Biology and Evolution, 30 (8), pp. 1843-1852. PDF [HT] [K] [Ch]

Pelletreau, K.N., Worful, J.M., Sarver, K.E., Rumpho, M.E. (2012) Laboratory culturing of Elysia chlorotica reveals a shift from transient to permanent kleptoplasty Symbiosis, 58 (1-3), pp. 221-232. Page1 [AQ] [F] [K] [Ch]

Middlebrooks, M.L., Bell, S.S., Pierce, S.K. (2012) The kleptoplastic sea slug Elysia clarki prolongs photosynthesis by synthesizing chlorophyll a and b. Symbiosis, 57 (3), pp. 127-132. Page1 [HT] [K] [Cl]

Pierce, S.K., Fang, X., Schwartz, J.A., Jiang, X., Zhao, W., Curtis, N.E., Kocot, K.M., Yang, B., Wang, J. (2012) Transcriptomic evidence for the expression of horizontally transferred algal nuclear genes in the photosynthetic sea slug, Elysia chlorotica. Molecular Biology and Evolution, 29 (6), pp. 1545-1556. PDF [HT] [K] [Ch]

Soule, K.M., Rumpho, M.E. (2012) Light-regulated photosynthetic gene expression and phosphoribulokinase enzyme activity in the heterokont alga Vaucheria litorea (xanthophyceae) and its symbiotic molluskan partner Elysia chlorotica (gastropoda). Journal of Phycology, 48 (2), pp. 373-383. Abstract [HT] [K] [Ch]

Schmitt, V., Wägele, H. (2011) Behavioral adaptations in relation to long-term retention of endosymbiotic chloroplasts in the sea slug Elysia timida (Opisthobranchia, Sacoglossa). Thalassas, 27 (2), pp. 225-238. PDF [BN] [K] [Ti]

Middlebrooks, M.L., Pierce, S.K., Bell, S.S. (2011) Foraging behavior under starvation conditions is altered via photosynthesis by the marine gastropod, Elysia clarki. PLoS ONE, 6 (7), art. no. e22162.  PDF [BN] [K] [Cl]

Wägele, H., Deusch, O., Händeler, K., Martin, R., Schmitt, V., Christa, G., Pinzger, B., Gould, S.B., Dagan, T., Klussmann-Kolb, A., Martin, W. (2011) Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes. Molecular Biology and Evolution, 28 (1), pp. 699-706. PDF [HT] [K] [Ti]

Rumpho, M.E., Pelletreau, K.N., Moustafa, A., Bhattacharya, D. (2011) The making of a photosynthetic animal. Journal of Experimental Biology, 214 (2), pp. 303-311. PDF [Aq] [HT] [K] [NH] [Ch]

Skulachev, V.P. (2010) Discovery of a photosynthesizing animal that can survive for months in a light-dependent manner. Biochemistry (Moscow), 75 (12), pp. 1498-1499. PDF [HT] [K] [R] [Ch]

Curtis, N.E., Schwartz, J.A., Pierce, S.K. (2010) Ultrastructure of sequestered chloroplasts in sacoglossan gastropods with differing abilities for plastid uptake and maintenance. Invertebrate Biology, 129 (4), pp. 297-308. Abstract [K] [Cl] [Ru] [Pt]

Schwartz, J.A., Curtis, N.E., Pierce, S.K. (2010) Using algal transcriptome sequences to identify transferred genes in the sea slug, Elysia chlorotica. Evolutionary Biology, 37 (1), pp. 29-37. PDF [HT] [K] [Ch]

Serôdio, J., Pereira, S., Furtado, J., Silva, R., Coelho, H., Calado, R. (2010) In vivo quantification of kleptoplastic chlorophyll a content in the “solar-powered” sea slug Elysia viridis using optical methods: Spectral reflectance analysis and PAM fluorometry. Photochemical and Photobiological Sciences, 9 (1), pp. 68-77. PDF [K] [Vi]

Pierce, S.K., Curtis, N.E., Schwartz, J.A. (2009) Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis, 49 (2), pp. 121-131.PDF [HT] [K] [Ch]

Händeler, K., Grzymbowski, Y.P., Krug, P.J., Wägele, H. (2009) Functional chloroplasts in metazoan cells – A unique evolutionary strategy in animal life. Frontiers in Zoology, 6 (1), art. no. 28. PDF [F] [K] [R]

Rumpho, M.E., Pochareddy, S., Worful, J.M., Summer, E.J., Bhattacharya, D., Pelletreau, K.N., Tyler, M.S., Lee, J., Manhart, J.R., Soule, K.M. (2009) Molecular characterization of the calvin cycle enzyme phosphoribulokinase in the stramenopile alga Vaucheria litorea and the plastid hosting mollusc Elysia chlorotica. Molecular Plant, 2 (6), pp. 1384-1396. PDF [HT] [K] [Ch]

Vieira, S., Calado, R., Coelho, H., Serôdio, J. (2009) Effects of light exposure on the retention of kleptoplastic photosynthetic activity in the sacoglossan mollusc Elysia viridis. Marine Biology, 156 (5), pp. 1007-1020. PDF [K] [Vi]

Evertsen, J., Johnsen, G. (2009) In vivo and in vitro differences in chloroplast functionality in the two north Atlantic sacoglossans (Gastropoda, Opisthobranchia) Placida dendritica and Elysia viridis. Marine Biology, 156 (5), pp. 847-859. PDF [K] [Vi]

Teugels, B., Bouillon, S., Veuger, B., Middelburg, J.J., Koedam, N. (2008) Kleptoplasts mediate nitrogen acquisition in the sea slug Elysia viridis. Aquatic Biology, 4 (1), pp. 15-21.PDF [K] [Vi]

Rumpho, M.E., Worful, J.M., Lee, J., Kannan, K., Tyler, M.S., Bhattacharya, D., Moustafa, A., Manhart, J.R. (2008) Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proceedings of the National Academy of Sciences of the United States of America, 105 (46), pp. 17867-17871. PDF [HT] [K] [Ch]

Casalduero, F.G., Muniain, C. (2008) The role of kleptoplasts in the survival rates of Elysia timida (Risso, 1818): (Sacoglossa: Opisthobranchia) during periods of food shortage. Journal of Experimental Marine Biology and Ecology, 357 (2), pp. 181-187. PDF [K] [Ti]

Pierce, S.K., Curtis, N.E., Hanten, J.J., Boerner, S.L., Schwartz, J.A. (2007) Transfer, integration and expression of functional nuclear genes between multicellular species. Symbiosis, 43 (2), pp. 57-64. [HT] [K] [Ch]

Schmitt, V., Anthes, N., Michiels, N.K. (2007) Mating behaviour in the sea slug Elysia timida (Opisthobranchia, Sacoglossa): Hypodermic injection, sperm transfer and balanced reciprocity. Frontiers in Zoology, 4, art. no. 17. [B] PDF [BN] [NH] [Ti]

Evertsen, J., Burghardt, I., Johnsen, G., Wägele, H. (2007) Retention of functional chloroplasts in some sacoglossans from the indo-pacific and Mediterranean. Marine Biology, 151 (6), pp. 2159-2166. PDF [K] [Pu] [Ti] [To]

Curtis, N.E., Pierce, S.K., Massey, S.E., Schwartz, J.A., Maugel, T.K. (2007) Newly metamorphosed Elysia clarki juveniles feed on and sequester chloroplasts from algal species different from those utilized by adult slugs. Marine Biology, 150 (5), pp. 797-806. PDF [AQ] [F] [K] [Cl]

Giménez Casalduero, F., Muniain, C. (2006) Photosynthetic activity of the solar-powered lagoon mollusc Elysia timida (Risso, 1818) (Opisthobranchia: Sacoglossa). Symbiosis, 41 (3), pp. 151-158. PDF [K] [Ti]

Pierce, S.K., Curtis, N.E., Massey, S.E., Bass, A.L., Karl, S.A., Finney, C.M. (2006) A morphological and molecular comparison between Elysia crispata and a new species of kleptoplastic sacoglossan sea slug (Gastropoda: Opisthobranchia) from the Florida Keys, USA.  Molluscan Research, 26 (1), pp. 23-38. Abstract [F] [K] [NH] [Cr] [Cl]

Curtis, N.E., Massey, S.E., Pierce, S.K. (2006) The symbiotic chloroplasts in the sacoglossan Elysia clarki are from several algal species. Invertebrate Biology, 125 (4), pp. 336-345.HTML [F] [K] [Cl]

Green, B.J., Fox, T.C., Rumpho, M.E. (2005) Stability of isolated algal chloroplasts that participate in a unique mollusc/kleptoplast association. Symbiosis, 40 (1), pp. 31-40. Abstract [K] [Ch]

Mondy, W.L., Pierce, S.K. (2003) Apoptotic-like morphology is associated with annual synchronized death in kleptoplastic sea slugs (Elysia chlorotica). Invertebrate Biology, 122 (2), pp. 126-137. Abstract [K] [NH] [Ch]

Hanten, J.J., Pierce, S.K. (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 (1), pp. 34-44.  PDF [K] [HT] [Ch]

Rumpho, M.E., Summer, E.J., Green, B.J., Fox, T.C., Manhart, J.R. (2001) 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? Zoology, 104 (3-4), pp. 303-312. Abstract [HT] [K] [Ch]

Muniain, C., Marín, A., Penchaszadeh, P.E. (2001) Ultrastructure of the digestive gland of larval and adult stages of the sacoglossan Elysia patagonica. Marine Biology, 139 (4), pp. 687-695. PDF [K] [Pa]

Trowbridge, C.D. (2000) The missing links: Larval and post-larval development of the ascoglossan opisthobranch Elysia viridis. Journal of the Marine Biological Association of the United Kingdom, 80 (6), pp. 1087-1094. Abstract [K] [NH] [Vi]

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 (1), pp. 331-342. Abstract PubMedCentral PDF [HT] [K] [Ch]

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, 197 (1), pp. 1-6. PDF [K] [NH] [Ch]

Mujer, C.V., Andrews, D.L., Manhart, J.R., Pierce, S.K., Rumpho, M.E. (1996) Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proceedings of the National Academy of Sciences of the United States of America, 93 (22), pp. 12333-12338. PubMedCentral PDF [HT] [K] [Ch]

Pierce, S.K., Biron, R.W., Rumpho, M.E. (1996) Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. Journal of Experimental Biology, 199 (10), pp. 2323-2330.  PDF [HT] [K] [Ch]

Carlini, D.B., Regan, J.D. (1995) Photolyase activities of Elysia tuca, Bursatella leachii, and Haminaea antillarum (Mollusca: Opisthobranchia). Journal of Experimental Marine Biology and Ecology, 189 (1-2), pp. 219-232. Abstract [NH] [K] [Tu]

Rumpho, M.E., Mujer, C.V., Andrews, D.L., Manhart, J.R., Pierce, S.K. (1994) Extraction of DNA from mucilaginous tissues of a sea slug (Elysia chlorotica). BioTechniques, 17 (6), pp. 1097-1101. Abstract [K] [Ch]

Brandley, B.K. (1984) Aspects of the ecology and physiology of Elysia cf. furvacauda ( Mollusca: Sacoglossa). Bulletin of Marine Science, 34 (2), pp. 207-219. Abstract [F] [K] [NH] [Fu]

Weaver, S., Clark, K.B. (1981) Light intensity and color preferences of five Ascoglossan = Sacoglossan) molluscs (Gastropoda: Opisthobranchia): a comparison of chloroplast symbiotic and aposymbiotic species.  Marine Behavior and Physiology, 7 pp. 297-306 Abstract [Bn] [K] [Cr] [Tu]

Rahat, M., Monelise, E.B. (1979) Photobiology of the chloroplast hosting mollusc Elysia timida. Journal of Experimental Biology 79, pp. 225-233.  PDF [BN] [K] [Ti]

Hinde, R. (1978) The metabolism of photosynthetically fixed carbon by isolated chloroplasts from Codium fragile (Chlorophyta: Siphonales) and by Elysia viridis (Mollusca: Sacoglossa).  Biological Journal of the Linnean Society, 10 (3), pp. 329-342. Abstract [F] [K] [Vi]

Deutch, B. (1978) Light-regulated body ion balance in marine slug Elysia viridis (Montagu). Nature, 274 (5667), pp. 159-160. Abstract [K] [Vi]

Trench, R.K., Boyle, J.E., Smith, D.C. (1974) The association between chloroplast of Codium fragile and the mollusc Elysia viridis. III. Movement of photosynthetically fixed 14C in tissues of intact living E. viridis and in Tridachia crispata. Proceedings of the Royal Society of London – Biological Sciences, 185 (1081), pp. 453-464. JStor PDF [K] [Cr] [Vi]

Trench, RK, RW Greene, BG Bystrom (1969) Chloroplasts as functional organelles in animal tissues J. Cell Biol.  42: 404-417  [F] [K] [Cr] [Di]

Hinde, R., Smith, D.C. (1972) Persistence of functional chloroplasts in Elysia viridis (Opisthobranchia, Sacoglossa). Nature: New biology, 239 (88), pp. 30-31. Abstract [K] [Vi]

Taylor, D.L. (1971) Photosynthesis of symbiotic chloroplasts in Tridachia crispata (Bërgh). Comparative Biochemistry and Physiology — Part A: Physiology, 38 (1), pp. 233-236. PDF [K] [Cr]

Greene, R.W. (1970) Symbiosis in sacoglossan opisthobranchs: functional capacity of symbiotic chloroplasts. Marine Biology, 7 (2), pp. 138-142. PDF [K] [He]

Trench, RK, ME Trench, L Muscatine (1972) Symbiotic chloroplasts; their photosynthetic products and contribution to mucus synthesis in two marine slugs The Biological Bulletin, 142 no. 2 335-349 [K] [Cr] [Di]

Trench, R.K. (1969) Chloroplasts as functional endosymbionts in the mollusc Tridachia crispata (Bërgh), (Opisthobranchia, Sacoglossa). Nature, 222 (5198), pp. 1071-1072. PDF [K] [Cr] [Paper chromatography of pigments]

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: 57-65.  [K] No abstract or PDF available.

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