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Retention of functional chloroplasts in some sacoglossans from the Indo-Pacific and Mediterranean

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Abstract

Previous studies on kleptoplasty in sacoglossans have used different methodology to investigate how long the sacoglossans are able to keep photosynthetically active (functional) chloroplasts. In this study we have used Pulse Amplitude Modulated Fluorometry to measure the quantum yield of charge separation in photosystem II in dark acclimated cells (ΦIIe) to detect the status of photosynthetic activity. Seven species of sacoglossa, Plakobranchus ocellatus, Elysia timida, Elysia sp, Elysia tomentosa, Thuridilla carlsoni, T. lineolata and Elysiella pusilla, were investigated regarding their ability to retain functional chloroplasts (RFC). The results show three different levels of RFC’s where P. ocellatus has the longest RFC for more than 11 months, E. timida with a RFC 1/4 than P. ocellatus (almost 3 months) and the rest with RFC’s down to 1/22 of P. ocellatus (up to 15 days). Based on these results, and compared to previous studies, eight different levels of retention abilities of non-functional and functional chloroplasts in sacoglossans are proposed. As far as we know, this is a novel method studying chloroplast functionality in sacoglossans.

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References

  • Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency on photosystems I and II in microalgae. Plant Physiol 110:689–696

    Article  CAS  Google Scholar 

  • Bjørkmann O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77k among vascular plants of diverse origins. Planta 170:489–504

    Article  Google Scholar 

  • Cha Y, Mauzerall DC (1992) Energy-storage of linear and cyclic electron flows in photosynthesis. Plant Physiol 100(4):1869–1877

    Article  CAS  Google Scholar 

  • Clark KB (1984) New records and synonymies of Bermuda opisthobranchs (Gastropoda). The Nautilus 98(2): 85–97

    Google Scholar 

  • 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 Mollusc Stud 44:272–282

    Google Scholar 

  • Clark KB, Jensen KR, Stirts HM (1990) Survey for functional kleptoplasty among West Atlantic Ascoglossa (= Sacoglossa) (Mollusca: Opisthobrachia). Veliger 33(4):339–345

    Google Scholar 

  • Demmig B, Bjørkman O (1987) Comparison of the effect of excessive light on chlorophyll fluoresence (77k) and photon yield of O-2 evolution in leaves of higher plants. Planta 171(2):171–184

    Article  CAS  Google Scholar 

  • Falkowski PG, Raven JA (1997) Aquatic photosynthesis. Blackwell, USA, p 375

    Google Scholar 

  • Genty B, Briantis JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160

    Article  CAS  Google Scholar 

  • Grant BR, Borowitzka MA (1984) The chloroplasts of giant celled and coenocytic algae: biochemistry and structure. Bot Rev 50(3):267–307

    Article  Google Scholar 

  • Greene RW (1970) Symbiosis in Sacoglossan opisthobranchs: functional capacity of symbiotic chloroplasts. Mar Biol 7(2):138–142

    Article  CAS  Google Scholar 

  • Hawes CR (1979) Ultrastructural aspects of the symbiosis between algal chloroplasts and Elysia viridis. New Phytol 83(2):445

    Article  Google Scholar 

  • Hinde R (1980) Chloroplast “symbiosis” in sacoglossans molluscs. In: Schwemmler W, Schenk HEA (eds) Endocytobiology, endosymbiosis and cell biology. Proceedings of the international colloquium on endosymbiosis and cell research. Tübingen, Germany, Walter de Gruyter, pp 729–36

  • Hinde R, Smith DC (1972) Persistence of functional chloroplasts in Elysia viridis (Opisthobranchia, Sacoglossa). Nature 239:30–31

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hinde R, Smih DC (1975) The role of photosynthesis in the nutrition of the mollusc Elysia viridis. Biol J Linn Soc 7:161–171

    Article  Google Scholar 

  • Ireland C, Scheuer PJ (1979) Photosynthetic marine molluscs: in vivo 14C incorporation into metabolites of the sacoglossan Plakobranchus ocellatus. Science 205(4409):922–923

    Article  CAS  Google Scholar 

  • Jensen KR (1980) A review of sacoglossan diets, with comparative notes on radular and buccal anatomy. Mal Rev 15:55–77

    Google Scholar 

  • Jensen KR (1992) Anatomy of some Indo-Pacific elysiidae (Opisthobranchia: Sacoglossa (= Ascoglossa)), with a discussion of the generic division and phylogeny. J Mollusc Stud 58:257–296

    Article  Google Scholar 

  • Jensen KR (1996) Phylogenetic systematics and classification of the Sacoglossa (Mollusca, Gastropoda, Opisthobranchia). Philos Trans R Soc Lond B 351:91–122

    Article  Google Scholar 

  • Jensen KR (1997) Evolution of the sacoglossa (Mollusca, Opisthobranchia) and the ecological associations with their food plants. Evol Ecol 11:301–335

    Article  Google Scholar 

  • Kolber Z, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38(8):1646–1665

    Article  CAS  Google Scholar 

  • van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Article  Google Scholar 

  • Kromkamp JC, Forster RM (2003) Use of variable fluorescence measurements in aquatic ecosystems: differences between multiple and single turnover measuring protocols and suggested terminology. Eur J Phycol 28(2):103–112

    Article  Google Scholar 

  • Marin A, Ros JD (1988) The Sacoglossa (Mollusca, Opisthobranchia) of South East Iberian peninsula. A catalogue of species and presence of algal chloroplasts in them. Iberius 8(1):25–49

    Google Scholar 

  • Marin A, Ros JD (1992) Dynamics of a peculiar plant–herbivore relationship: the photosynthetic ascoglossan Elysia timida and the chlorophycean Acetabularia acetabulum. Mar Biol 112:677–682

    Article  Google Scholar 

  • Rumpho ME, Summer EJ, Manhart JR (2000) Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol 123:29–38

    Article  CAS  Google Scholar 

  • Taylor DL (1968) Chloroplasts as symbiotic organelles in the digestive gland of Elysia viridis (Gastropoda: Opisthobranchia). J Mar Biol Assoc UK 48:1–15

    Article  Google Scholar 

  • Trench RK (1969) Chloroplasts as functional endosymbionts in the mollusc Tridachia crispata (Bergh), (Opisthobranchia, Sacoglossa). Nature 22:1071–1072

    Article  Google Scholar 

  • Trench RK (1975) Of ‘leaves that crawl’. Functional chloroplasts in animal cells. Symp Soc Exp Biol 29:229–265

    CAS  Google Scholar 

  • Trench RK, Smith DC (1970) Synthesis of pigment in symbiotic chloroplasts. Nature 227:196–197

    Article  CAS  Google Scholar 

  • 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. Proc R Soc Lond B 184:63–81

    Article  CAS  Google Scholar 

  • Trench RK, Olhorst S (1976) The stability of chloroplasts from siphonaceous algae in symbiosis with sacoglossan mollusca. New Phytol 76:99–109

    Article  CAS  Google Scholar 

  • Wägele H, Johnsen G (2001) Observations on the histology and photosynthetic performance of “solar powered” opisthobranchs (Mollusca, Gastropoda, Opisthobranchia) containing symbiotic chloroplasts or zooxanthellae. Org Divers Evol 1:193–210

    Article  Google Scholar 

  • Waugh GR, Clark KB (1986) Seasonal and geographic variation in chlorophyll level of Elysia tuca (Ascoglossa: Opisthobranchia). Mar Biol 92:483–487

    Article  Google Scholar 

  • Williams SI, Walker DI (1999) Mesoherbivore–macroalgal interactions: feeding ecology of sacoglossan sea slugs (Mollusca, Opisthobranchia) and their effects on their food algae. Oceanogr Mar Biol Annu Rev 37:87–138

    Google Scholar 

Download references

Acknowledgments

We would like to thank colleagues and staff at Lizard Island Research Station (Australia), and at the Faculty of Fisheries & Marine Science at the Sam Ratulangi University Manado (Sulawesi, Indonesia). This study was supported by the German Science Foundation to I. Burghardt and H. Wägele (SSP 1127: Wa 618/8) and by “The Improving Human Potential – Transnational Access to Research Infrastructures Programme of the European Commission” in Trondheim, Norway, and by the Norwegian Research Council to J. Evertsen (NFR 153790/120). Experiments comply with the current laws of the countries in which the experiments were performed.

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Authors and Affiliations

  1. Department of Biology, Norwegian University of Technology and Science, Trondhjem Biological Station, Bynesveien 46, Trondheim, 7491, Norway

    Jussi Evertsen & Geir Johnsen

  2. Spezielle Zoologie, Ruhr-Universität Bochum, Bochum, Germany

    Ingo Burghardt

  3. Institut für Evolutionsbiologie und Ökologie and Zoologisches Forschungsmuseum König, University of Bonn, Bonn, Germany

    Heike Wägele

Authors
  1. Jussi Evertsen
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  2. Ingo Burghardt
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  3. Geir Johnsen
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  4. Heike Wägele
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Correspondence to Jussi Evertsen.

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Communicated by M. Kühl.

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Evertsen, J., Burghardt, I., Johnsen, G. et al. Retention of functional chloroplasts in some sacoglossans from the Indo-Pacific and Mediterranean. Mar Biol 151, 2159–2166 (2007). https://doi.org/10.1007/s00227-007-0648-6

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  • DOI: https://doi.org/10.1007/s00227-007-0648-6

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