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Effects of light exposure on the retention of kleptoplastic photosynthetic activity in the sacoglossan mollusc Elysia viridis

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Abstract

The effects of light exposure on the photosynthetic activity of kleptoplasts were studied in the sacoglossan mollusc Elysia viridis. The photosynthetic activity of ingested chloroplasts was assessed in vivo by non-destructively measuring photophysiological parameters using pulse amplitude modulation (PAM) fluorometry. Animals kept under starvation were exposed to two contrasting light conditions, 30 μmol photons m−2 s−1 (low light, LL), and 140 μmol photons m−2 s−1 (high light, HL), and changes in photosynthetic activity were monitored by measuring the maximum quantum yield of photosystem II (PSII), Fv/Fm, the minimum fluorescence, Fo, related to chlorophyll a content, and by measuring rapid light-response curves (RLC) of relative electron transport rate (rETR). RLCs were characterised by the initial slope of the curve, αRLC, related to efficiency of light capture, and the maximum rETR level, rETRm,RLC, determined by the carbon-fixation metabolism. Starvation induced the decrease of all photophysiological parameters. However, the retention of photosynthetic activity (number of days for Fv/Fm > 0), as well as the rate and the patterns of its decrease over time, varied markedly with light exposure. Under HL conditions, a rapid, exponential decrease was observed for Fv/Fm, αRLC and rETRm,RLC, Fo not showing any consistent trend of variation, and retention times ranged between 6 and 15 days. These results suggested that the retention of chloroplast functionality is limited by photoinactivation of PSII reaction center protein D1. In contrast, under LL conditions, a slower decrease in all parameters was found, with retention times varying from 15 to 57 days. Fv/Fm, αRLC and rETRm,RLC exhibited a bi-phasic pattern composed by a long phase of slow decrease in values followed by a rapid decline, whilst Fo decayed exponentially. These results were interpreted as resulting from lower rates of D1 photoinactivation under low light and from the gradual decrease in carbon provided by photosynthesis due to reduction of functional photosynthetic units.

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References

  • Carr H, Björk M (2007) Parallel changes in non-photochemical quenching properties, photosynthesis and D1 levels at sudden, prolonged irradiance exposures in Ulva fasciata Delile. J Photochem Photobiol B 87:18–26. doi:https://doi.org/10.1016/j.jphotobiol.2006.12.005

    Article  CAS  Google Scholar 

  • Chow W, Aro E-M (2005) Photoinactivation and mechanisms of recovery. In: Wydrzynski TJ, Satoh K, Freeman JA (eds) Photosystem II: the light-drivenwater: plastoquinone oxidoreductase. Springer, Dordrecht, pp 628–648

    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 Molluscan Stud 44:272–282

    Google Scholar 

  • Clark KB, Defreese D (1987) Population ecology of Caribbean ascoglossa (mollusca: opisthobranchia): a study of specialized herbivores. Am Malacol Bull 5:259–280

    Google Scholar 

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

    Google Scholar 

  • Cobb AH (1978) Inorganic polyphosphate involved in the symbiosis between chloroplasts of alga Codium fragile and mollusc Elysia viridis. Nature 272:554–555. doi:https://doi.org/10.1038/272554a0

    Article  CAS  Google Scholar 

  • Cruz S, Serôdio J (2008) Relationship of rapid light curves of variable fluorescence to photoacclimation and non-photochemical quenching in a benthic diatom. Aquat Bot 88:256–264

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Falkowski PG, Raven JA (1997) Aquatic photosynthesis. Blackwell, Oxford

    Google Scholar 

  • Falkowski PG, Greene R, Kolber Z (1994) Light utilization and photoinhibition of photosynthesis in marine phytoplankton. In: Baker NR, Bowes J (eds) Photoinhibition of photosynthesis: from molecular mechanisms to the field. Bios Scientific, Oxford, pp 407s–432s

    Google Scholar 

  • Figueroa FL, Conde-Alvarez R, Gomez I (2003) Relations between electron transport rates determined by pulse amplitude modulated chlorophyll fluorescence and oxygen evolution in macroalgae under different light conditions. Photosynth Res 75:259–275. doi:https://doi.org/10.1023/A:1023936313544

    Article  CAS  Google Scholar 

  • Franklin LA, Badger MR (2001) A comparison of photosynthetic electron transport rates in macroalgae measured by pulse amplitude modulated chlorophyll fluorometry and mass spectrometry. J Phycol 37:756–767. doi:https://doi.org/10.1046/j.1529-8817.2001.00156.x

    Article  CAS  Google Scholar 

  • Genty B, Briantais J-M, 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 

  • Giménez-Casalduero F, Muniain C (2006) Photosynthetic activity of the solar-powered lagoon mollusc Elysia timida (Risso, 1818) (Opisthobranchia: Sacoglossa). Symbiosis 41:151–158

    Google Scholar 

  • Giménez-Casalduero F, Muniain C (2008) The role of kleptoplasts in the survival rates of Elysia timida (Risso, 1818): (Sacoglossa: Opisthobranchia) during periods of food shortage. J Exp Mar Biol Ecol 357:181–187. doi:https://doi.org/10.1016/j.jembe.2008.01.020

    Article  Google Scholar 

  • Goto N, Miyazaki H, Nakamura N, Terai H, Ishida N, Mitamura O (2008) Relationships between electron transport rates determined by pulse amplitude modulated (PAM) chlorophyll fluorescence and photosynthetic rates by traditional and common methods in natural freshwater phytoplankton. Fund Appl Limnol 172:121–134. doi:https://doi.org/10.1127/1863-9135/2008/0172-0121

    Article  CAS  Google Scholar 

  • Green BJ, Li W-Y, Manhart JR, Fox TC, Summer EJ, Kennedy RA, Pierce SK, Rumpho ME (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 Physiol 124:331–342. doi:https://doi.org/10.1104/pp.124.1.331

    Article  CAS  Google Scholar 

  • Greene RW (1970) Symbiosis in Sacoglossan opisthobranchs: functional capacity of symbiotic chloroplasts. Mar Biol (Berl) 7:138–142. doi:https://doi.org/10.1007/BF00354917

    Article  CAS  Google Scholar 

  • Hartig P, Wolfstein K, Lippemeier S, Colijn F (1998) Photosynthetic activity of natural microphytobenthos populations measured by fluorescence (PAM) and 14C-tracer methods: a comparison. Mar Ecol Prog Ser 166:53–62. doi:https://doi.org/10.3354/meps166053

    Article  Google Scholar 

  • Hawes CR (1979) Ultrastructural aspects of the symbiosis between algal chloroplasts and Elysia viridis. New Phytol 83:445–450. doi:https://doi.org/10.1111/j.1469-8137.1979.tb07469.x

    Article  Google Scholar 

  • Hinde R, Smith DC (1975) The role of photosynthesis in the nutrition of the mollusc Elysia viridis. Biol J Linn Soc Lond 7:161–171. doi:https://doi.org/10.1111/j.1095-8312.1975.tb00738.x

    Article  Google Scholar 

  • Hinde R, Smith DC (1972) Persistence of functional chloroplasts in Elysia viridis (Opisthobranchia, Sacoglossa). Nature 239:30–31. doi:https://doi.org/10.1038/239041a0

    Article  CAS  Google Scholar 

  • Honeywill C, Hagerthey SE, Paterson DM (2002) Determination of microphytobenthic biomass using pulse–amplitude modulated minimum fluorescence. Eur J Phycol 37:485–492. doi:https://doi.org/10.1017/S0967026202003888

    Article  Google Scholar 

  • Ireland C, Scheuer PJ (1979) Photosynthetic marine molluscs: in vivo 14C incorporation into metabolites of the sacoglossan Plakobranchus ocellatus. Science 205:922–923. doi:https://doi.org/10.1126/science.205.4409.922

    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 (1997) Evolution of the sacoglossa (Mollusca, Opisthobranchia) and the ecological associations with their food plants. Evol Ecol 11:301–335. doi:https://doi.org/10.1023/A:1018468420368

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lavaud J, Rousseau B, van Gorkom HJ, Etienne AL (2002) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol 129:1398–1406. doi:https://doi.org/10.1104/pp.002014

    Article  CAS  Google Scholar 

  • Lee H-Y, Hong Y-N, Chow WS (2001) Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves. Planta 212:332–342. doi:https://doi.org/10.1007/s004250000398

    Article  CAS  Google Scholar 

  • Marín A, Ros JD (2004) Chemical defenses in sacoglossan opisthobranchs: taxonomic trends and evolutive implications. Sci Mar 68:227–241. doi:https://doi.org/10.3989/scimar.2004.68s1227

    Article  Google Scholar 

  • 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 USA 93:12333–12338. doi:https://doi.org/10.1073/pnas.93.22.12333

    Article  CAS  Google Scholar 

  • Muniain C, Marín A, Penchaszadeh P (2001) Ultrastructure of the digestive gland of larval and adult stages of the sacoglossan Elysia patagonica. Mar Biol (Berl) 139:687–695. doi:https://doi.org/10.1007/s002270100622

    Article  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359. doi:https://doi.org/10.1146/annurev.arplant.50.1.333

    Article  CAS  Google Scholar 

  • Perkins RG, Mouget J-L, Lefebvre S, Lavaud J (2006) Light response curve methodology and possible implications in the application of chlorophyll fluorescence to benthic diatoms. Mar Biol (Berl) 149:703–712. doi:https://doi.org/10.1007/s00227-005-0222-z

    Article  Google Scholar 

  • Pierce SK, Biron RW, Rumpho ME (1996) Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J Exp Biol 199:2323–2330

    CAS  PubMed  Google Scholar 

  • Platt T, Gallegos CL, Harison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701

    Google Scholar 

  • Queiroga H, Almeida MJ, Alpuim T, Flores AAV, Francisco S, Gonzalez-Gordillo JI, Miranda AI, Silva I, Paula J (2006) Wind and tide control of megalopal supply to estuarine crab populations on the Portuguese west coast. Mar Ecol Prog Ser 307:21–36. doi:https://doi.org/10.3354/meps307021

    Article  Google Scholar 

  • Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237. doi:https://doi.org/10.1016/j.aquabot.2005.02.006

    Article  CAS  Google Scholar 

  • Raven JA, Walker DI, Jensen KR, Handley LL, Scrimgeour CM, McInroy SG (2001) What fraction of the organic carbon in sacoglossans is obtained from photosynthesis by kleptoplastids? An investigation using the natural abundance of stable carbon isotopes. Mar Biol (Berl) 138:537–545. doi:https://doi.org/10.1007/s002270000488

    Article  CAS  Google Scholar 

  • Rudman WB (1982) The taxonomy and biology of further aeolidacean and arminacean nudibranch molluscs with symbiotic zooxanthellae. Zool J Linn Soc Lond 74:147–196. doi:https://doi.org/10.1111/j.1096-3642.1982.tb01146.x

    Article  Google Scholar 

  • Rumpho ME, Summer EJ, Manhart JR (2000) Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol 123:29–38. doi:https://doi.org/10.1104/pp.123.1.29

    Article  CAS  Google Scholar 

  • 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. doi:https://doi.org/10.1078/0944-2006-00036

    Article  CAS  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62. doi:https://doi.org/10.1007/BF00024185

    Article  CAS  Google Scholar 

  • Schreiber U, Gademann R, Ralph PJ, Larkum AWD (1997) Assessment of photosynthetic performance of Prochloron in Lissoclinum patella in hospite by chlorophyll fluorescence measurements. Plant Cell Physiol 38:945–951

    Article  CAS  Google Scholar 

  • Serôdio J, Marques da Silva J, Catarino F (1997) Nondestructive tracing of migratory rhythms of intertidal microalgae using in vivo chlorophyll a fluorescence. J Phycol 33:542–553. doi:https://doi.org/10.1111/j.0022-3646.1997.00542.x

    Article  Google Scholar 

  • Serôdio J, Vieira S, Cruz S, Barroso F (2005) Short-term variability in the photosynthetic activity of microphytobenthos as detected by measuring rapid light curves using variable fluorescence. Mar Biol (Berl) 146:903–914. doi:https://doi.org/10.1007/s00227-004-1504-6

    Article  Google Scholar 

  • Serôdio J, Vieira S, Cruz S, Coelho H (2006) Rapid light-response curves of chlorophyll fluorescence in microalgae: relationship to steady-state light curves and non-photochemical quenching in benthic diatom-dominated assemblages. Photosynth Res 90:29–43. doi:https://doi.org/10.1007/s11120-006-9105-5

    Article  Google Scholar 

  • Serôdio J, Vieira S, Barroso F (2007) Relationship of variable chlorophyll fluorescence indices to photosynthetic rates in microphytobenthos. Aquat Microb Ecol 49:71–85. doi:https://doi.org/10.3354/ame01129

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. WH Freeman, New York

    Google Scholar 

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

    Article  Google Scholar 

  • Trench RK, Olhorst S (1976) The stability of chloroplasts from siphonaceous algae in symbiosis with sacoglossan mollusca. New Phytol 76:99–109. doi:https://doi.org/10.1111/j.1469-8137.1976.tb01442.x

    Article  CAS  Google Scholar 

  • Trench RK, Smith DC (1970) Synthesis of pigment in symbiotic chloroplasts. Nature 227:196–197. doi:https://doi.org/10.1038/227196a0

    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 Biol Sci 184:63–81

    Article  CAS  Google Scholar 

  • Tyystjärvi E, Aro E-M (1996) The rate constant of photoinhibition measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93: 22-13-2218

    Article  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. doi:https://doi.org/10.1078/1439-6092-00016

    Article  Google Scholar 

  • Waugh GR, Clark KB (1986) Seasonal and geographic variation in chlorophyll level of Elysia tuca (Ascoglossa: Opisthobranchia). Mar Biol (Berl) 92:483–487. doi:https://doi.org/10.1007/BF00392508

    Article  Google Scholar 

  • White AJ, Critchley C (1999) Rapid light curves: a new fluorescence method to assess the state of the photosynthetic apparatus. Photosynth Res 59:63–72. doi:https://doi.org/10.1023/A:1006188004189

    Article  CAS  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 

  • Yamagushi K, Mayfield SP (2005) Transcriptional and translational regulation of photosystem II gene expression. In: Wydrzynski TJ, Satoh K, Freeman JA (eds) Photosystem II: the light-drivenwater: plastoquinone oxidoreductase. Springer, Dordrecht, pp 649–668

    Google Scholar 

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Acknowledgments

We would like to express our gratitude to Sílvia Pereira, Ana Sequeira and Henrique Queiroga who provided us the specimens analysed in the present study, collected as part of the daily sampling programme of Carcinus maenas megalopae financed by project PTDC/BIA-BDE/65425/2006. We also thank Estibaliz Berecibar for help in the identification of the Codium species. The experiments in the present work comply with the current laws of the country in which these experiments were performed.

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Correspondence to João Serôdio.

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Vieira, S., Calado, R., Coelho, H. et al. Effects of light exposure on the retention of kleptoplastic photosynthetic activity in the sacoglossan mollusc Elysia viridis . Mar Biol 156, 1007–1020 (2009). https://doi.org/10.1007/s00227-009-1144-y

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