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Phagocytosis of algal chloroplasts by digestive gland cells in the photosynthesis-capable slug Elysia timida (Mollusca, Opisthobranchia, Sacoglossa)

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Abstract

Parapodia of the sacoglossan slug Elysia timida were preserved by high-pressure cryofixation during feeding experiments and investigated with transmission electron microscopy. This slug has been known for its long-term retention of active chloroplasts and photosynthesis. We observed different stages of phagocytosis of chloroplast components from ingested algal food by slug digestive gland cells. Thylakoid stacks and stroma of chloroplasts were engulfed by the slug cells. In the slug cells thylakoids were surrounded by one membrane only. This membrane is interpreted as having been generated by the mollusk during phagocytosis. It is inferred to be eukaryotic in origin and unlikely, therefore, to be endowed with the translocons system ordinarily regulating import of algal gene-encoded plastid preproteins. Our structural findings suggest that chloroplast components in the slug cells are thylakoid stacks with chloroplast stroma only.

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References

  1. Bourett TM, Czymmek KJ, Howard RJ (1999) Ultrastructure of chloroplast protuberances in rice leaves preserved by high-pressure freezing. Planta 208:472–479

  2. 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. Mar Biol 156:847–859

  3. Giménez-Casalduero F, Muniain C, González-Wangüemert M, Garrote-Moreno A (2011) Elysia timida (Risso,1818) three decades of research. Anim Biodivers Conserv 34:217–227

  4. Graves DA, Gibson MA, Bleakney JS (1979) The digestive diverticula of Alderia modesta and Elysia chlorotica (Opisthobranchia: Sacoglossa). Veliger 21:415–422

  5. Händeler K, Grzymbowski YP, Krug PJ, Wägele H (2009) Functional chloroplasts in metazoan cells—a unique evolutionary strategy in animal life. Frontiers Zool 6:28–45

  6. Lopez-Juez E (2007) Plastid biogenesis, between light and shadows. J Exp Bot 5:11–26

  7. Marin A, Ros J (1993) Ultrastructural and ecological aspects of the development of chloroplast retention in the sacoglossan gastropod Elysia timida. J Mol Studies 59:95–104

  8. McLean N (1976) Phagocytosis of chloroplasts in Placida dendritica (Gastropoda: Sacoglossa). J Exp Zool 197:321–330

  9. Menzel D (1994) An interconnected plastidom in Acetabularia: implications for the mechanism of chloroplast motility. Protoplasma 179:166–171

  10. Müller M, Moor H (1984) Cryofixation of suspensions and tissue by propane jet freezing and high pressure freezing. In: Bailey GW (ed) Proceedings of 42nd annual meeting on Electron Microscope Society of America. CA, San Francisco

  11. Natesan SKA, Sullivan JA, Gray JC (2005) Stromules: a characteristic cell-specific feature of plastid morphology. J Exp Bot 56:787–797

  12. Pierce SK, Curtis NE (2012) The cell biology of the chloroplast symbiosis in sacoglossan sea slugs. Intern Rev Cell Mol Biol 293:123–148

  13. Pierce SK, Xiaodong F, Schwartz JA, Xuanting J, Zhao Wei, Curtis NE, Kocot KM, Bicheng Y, Jian W (2012) Transcriptomic evidence for the expression of horizontally transferred algal nuclear genes in the photosynthetic sea slug, Elysia chlorotica. Mol Biol Evol 29(6):1545–1556

  14. Rumpho ME, Summer EJ, Manhart JR (2000) Solar-powered sea slugs. Plant Physiol 123:29–38

  15. Rumpho ME, Summer EJ, Green BJ, Fox TC, Manhart JR (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 104:303–312

  16. Rumpho ME, Dastoor FP, Manhart JR, Lee J (2007) The kleptoplast. In: Wise RA, Hoober JK (eds) The structure and function of plastids, pp 451–473

  17. Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhattacharya D, Moustafa A, Manhart JR (2008) Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc Nat Acad Sci USA 105:17867–17871

  18. Rumpho ME, Pelletreau KN, Moustafa A, Bhattacharya D (2011) The making of a photosynthetic animal. J Exp Biol 214:303–311

  19. Schwartz JA, Curtis NE, Pierce SK (2010) Using algal transcriptome sequences to identify transferred genes in the sea slug, Elysia chlorotica. Evol Biol 37:29–37

  20. Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Rev Genet 5:123–135

  21. Touret N, Paroutis P, Grinstein S (2005) The nature of the phagosomal membrane: endoplasmic reticulum versus plasmalemma. J Leucocyte Biol 77:878–885

  22. Wägele H, Deusch O, Händeler K, Martin R, Schmitt V, Christa G, Pinzger B, Gould SB, Dagan T, Klussman-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. Mol Biol Evol 28:699–706

  23. Walther P, Ziegler A (2002) Freeze substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water. J Microsc 208:3–10

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Acknowledgments

We would like to thank Eberhard Schmid and Dr. Katharina Höhn for assistance in high-pressure cryofixation and freeze substitution of the samples. Dipl. biol. Valerie Schmitt supplied living specimens from Banyuls-sur-mer (France) under various conditions, after fasting and light exposition, or freshly fed and helped to prepare tissues for cryofixation. Prof. Edward Koenig (Buffalo, USA) critically read and revised the manuscript.

Author information

Correspondence to Rainer Martin.

Additional information

Communicated by A. Schmidt-Rhaesa.

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Martin, R., Walther, P. & Tomaschko, K. Phagocytosis of algal chloroplasts by digestive gland cells in the photosynthesis-capable slug Elysia timida (Mollusca, Opisthobranchia, Sacoglossa). Zoomorphology 132, 253–259 (2013). https://doi.org/10.1007/s00435-012-0184-x

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Keywords

  • Kleptoplasty
  • Mollusk cells
  • Membranes
  • High-pressure cryofixation
  • Ultrastructure