Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-24T13:27:46.477Z Has data issue: false hasContentIssue false
  • English
  • Français

Photobiology of the symbiotic acoel flatworm Symsagittifera roscoffensis: algal symbiont photoacclimation and host photobehaviour

Published online by Cambridge University Press:  14 July 2010

João Serôdio ,
Raquel Silva ,
João Ezequiel  and
Ricardo Calado
João Serôdio*
Affiliation:
Departamento de Biologia and CESAM—Centro de Estudos do Ambiente e do Mar, Universidade de Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal
Raquel Silva
Affiliation:
Departamento de Biologia and CESAM—Centro de Estudos do Ambiente e do Mar, Universidade de Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal
João Ezequiel
Affiliation:
Departamento de Biologia and CESAM—Centro de Estudos do Ambiente e do Mar, Universidade de Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal
Ricardo Calado
Affiliation:
Departamento de Biologia and CESAM—Centro de Estudos do Ambiente e do Mar, Universidade de Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal
*
Correspondence should be addressed to: J. Serôdio, Departamento de Biologia and CESAM—Centro de Estudos do Ambiente e do Mar, Universidade de Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The symbiotic association between the acoel flatworm Symsagittifera roscoffensis and the prasinophyte microalgae Tetraselmis convolutae was studied regarding its photophysiology and photobehaviour. The photoacclimation status and the photophysiological responses to high light of the algal endosymbiont were studied non-destructively on individual S. roscoffensis using pulse amplitude modulated fluorometry. Specimens collected in an intertidal sandy shore were characterized regarding the maximum quantum yield of photosystem II (PSII), Fv/Fm, and the light response of photosynthetic activity, by constructing rapid light-response curves of the relative electron transport rate of PSII, rETR. The studied population could be considered as high light-acclimated when compared with other intertidal photosynthetic organisms (e.g. macroalgae), with the light-saturation parameter Ek averaging 250 μmol m−2 s−1. Light stress experiments showed S. roscoffensis to be able to withstand the exposure to high light without displaying signs of photoinhibition, suggesting the operation of efficient physiological photoprotective processes. The photobehaviour of S. roscoffensis was studied by characterizing the distribution of the flatworms under a light gradient, using a custom-made photoaccumulation chamber. The results showed a photoaccumulation pattern evidencing a clear avoidance of extreme low or high light levels, and with maximum photoaccumulation values being found for a range of irradiances (150–400 μmol m−2 s−1) that generally coincided with the optima for photosynthetic activity. This matching between the optimum light levels for photosynthetic activity and photoaccumulation suggested that S. roscoffensis may use vertical migration as a form of behavioural photoprotection. This behavioural response may be used to rapidly and flexibly control light exposure, avoiding photodamage to the endosymbiont photosynthetic apparatus by direct exposure to sunlight.

Keywords

photosynthetic symbiosesphotoacclimationphotoprotectionphotobehaviourchlorophyll fluorescenceacoelSymsagitifferaTetraselmis
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 1 , February 2011 , pp. 163 - 171
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arsalane, W., Rousseau, B. and Duval, J.C. (1994) Influence of the pool size of the xanthophyll cycle on the effects of light stress in diatoms: competition between photoprotection and photoinhibition. Photochemistry and Photobiology 60, 237–243.CrossRefGoogle Scholar
Behrenfeld, M.J., Prasil, O., Babin, M. and Bruyant, F. (2004) In search of a physiological basis for covariations in light-limited and light-saturated photosynthesis. Journal of Phycology 40, 4–25.CrossRefGoogle Scholar
Boyle, J.E. and Smith, D.C. (1975) Biochemical interactions between the symbionts of Convoluta roscoffensis. Proceedings of the Royal Society of London (Series B) 189, 131–135.Google Scholar
Doonan, S.A. and Gooday, G.W. (1982) Ecological studies of symbiosis in Convoluta roscoffensis. Marine Ecology Progress Series 8, 69–73.CrossRefGoogle Scholar
Douglas, A.E. (1992) Algal symbioses in acoel turbellaria: factors determining the identity of the algal symbionts. In Reisser, W. (ed.) Algae and symbiosis. Bristol: Biopress Limited, pp. 199–214.Google Scholar
Falkowski, P.G., Greene, R. and Kolber, Z. (1994) Light utilization and photoinhibition of photosynthesis in marine phytoplankton. In Baker, N.R. and Bowes, J. (eds) Photoinhibition of photosynthesis: from molecular mechanisms to the field. Oxford: Bios Scientific, pp. 407–432.Google Scholar
Furukawa, T., Watanabe, M. and Shihira-Ishikawa, I. (1998) Green- and blue-light-mediated chloroplast migration in the centric diatom Pleurosira laevis. Protoplasma 203, 214–220.CrossRefGoogle Scholar
Genty, B., Briantais, J.-M. and Baker, N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.CrossRefGoogle Scholar
Gévaert, F., Créach, A., Davoult, D., Migné, A., Levavasseur, G., Arzel, P., Holl, A.C. and Lemoine, Y. (2003). Laminaria saccharina photosynthesis measured in situ: photoinhibition and xanthophyll cycle during a tidal cycle. Marine Ecology Progress Series 247, 43–50.CrossRefGoogle Scholar
Giménez-Casalduero, F. and 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, 181–187.CrossRefGoogle Scholar
Hofstraat, J.W., Peeters, J.C.H., Snel, J.F.H. and Geel, C. (1994) Simple determination of photosynthetic efficiency and photoinhibition of Dunaliella tertiolecta by saturating pulse fluorescence measurements. Marine Ecology Progress Series 103, 187–196.CrossRefGoogle Scholar
Holligan, P.M. and Gooday, G.W. (1975) Symbiosis in Convoluta roscoffensis. In Jennings, D.H. and Lee, D.L. (eds) Symbiosis. Cambridge: Cambridge University Press, pp. 205–227 [Symposium of the Society of Experimental Biology, Volume 29]Google ScholarPubMed
Kasahara, M., Kagawa, T., Iokawa, K., Suetsugu, N., Miyao, M. and Wada, M. (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420, 829–832.CrossRefGoogle ScholarPubMed
Kremer, B.P. (1975) 14CO2-fixation by the endosymbiotic alga Platymonas convolutae within the turbellarian Convoluta roscoffensis. Marine Biology 31, 219–226.CrossRefGoogle Scholar
Lavaud, J., Rousseau, B., van Gorkom, H.J. and Etienne, A.L. (2002) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiology 129, 1398–1406.CrossRefGoogle ScholarPubMed
MacIntyre, H.L., Kana, T.M., Anning, T. and Geider, R.J. (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. Journal of Phycology 38, 17–38.CrossRefGoogle Scholar
McCoy, A.M. and Balzer, I. (2002) Algal symbiosis in flatworms. In Seckbach, J. (ed.) Symbiosis: mechanisms and models systems. Dordrecht: Kluwer, pp. 561–574.Google Scholar
Meyer, H., Provasoli, L. and Meyer, F. (1979) Lipid biosynthesis in the marine flatworm Convoluta roscoffensis and its algal symbiont Platymonas convoluta. Biochimica et Biophysica Acta 573, 464–480.CrossRefGoogle ScholarPubMed
Müller, P., Li, X.-P. and Niyogi, K. (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.CrossRefGoogle ScholarPubMed
Muscatine, L., Boyle, J.E. and Smith, D.C. (1974) Symbiosis of the acoel flatworm Convoluta roscoffensis with the alga Platymonas convolutae. Proceedings of the Royal Society of London (Series B) 187, 221–234.Google ScholarPubMed
Nozawa, K., Taylor, D.L. and Provasoli, L. (1972) Respiration and photosynthesis in Convoluta roscoffensis Graff, infected with various symbionts. Biological Bulletin. Marine Biological Laboratory, Woods Hole 143, 420–430.CrossRefGoogle ScholarPubMed
Olaizola, M. and Yamamoto, H.Y. (1994) Short-term response of the diadinoxanthin cycle and fluorescence yield to high irradiance in Chaetoceros muelleri (Bacillariophyceae). Journal of Phycology 30, 606–612.CrossRefGoogle Scholar
Perkins, R.G., Mouget, J.-L., Lefebvre, S. and Lavaud, J. (2006) Light response curve methodology and possible implications in the application of chlorophyll fluorescence to benthic diatoms. Marine Biology 149, 703–712.CrossRefGoogle Scholar
Platt, T., Gallegos, C.L. and Harrison, W.G. (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal of Marine Research 38, 687–701.Google Scholar
Ralph, P.J., Gademann, R., Larkum, A.W.D. and Schreiber, U. (1999) In situ underwater measuremens of photosynthetic activity of coral zooxanthellae and other reef-dwelling dinoflagellate endosymbionts. Marine Ecology Progress Series 180, 139–147.CrossRefGoogle Scholar
Ralph, P.J., Gademann, R., Larkum, A.W.D. and Kühl, M. (2002) Spatial heterogeneity in active chlorophyll fluorescence and PSII activity of coral tissues. Marine Biology 141, 639–646.Google Scholar
Reisser, W. and Hader, D.P. (1984) Role of endosymbiotic algae in photokinesis and photophobic responses of ciliates. Photochemistry and Photobiology 39, 673–678.CrossRefGoogle Scholar
Ruiz-Trillo, I., Ruitort, M., Littlewood, D.T.J., Herniou, E.A. and Baguñà, J. (1999) Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science 283, 1919–1923.CrossRefGoogle Scholar
Schreiber, U., Schliwa, U. and Bilger, W. (1986) Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research 10, 51–62.CrossRefGoogle ScholarPubMed
Schreiber, U., Bilger, W. and Neubauer, C. (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In Shulze, E.D. and Caldwell, M.M. (eds) Ecophysiology of photosynthesis. Berlin: Springer, pp 49–70.Google Scholar
Schreiber, U., Gademann, R., Ralph, P.J. and Larkum, A.W.D. (1997) Assessment of photosynthetic performance of Prochloron in Lissoclinum patella in hospite by chlorophyll fluorescence measurements. Plant Cell Physiology 38, 945–951.CrossRefGoogle Scholar
Serôdio, J., Cruz, S., Vieira, S. and Brotas, V. (2005) Non-photochemical quenching of chlorophyll fluorescence and operation of the xanthophyll cycle in estuarine microphytobenthos. Journal of Experimental Marine Biology and Ecology 326, 157–169.CrossRefGoogle Scholar
Serôdio, J., Coelho, H., Vieira, S. and Cruz, S. (2006a) Microphytobenthos vertical migratory photoresponse as characterised by light-response curves of surface biomass. Estuarine, Coastal and Shelf Science 68, 547–556.CrossRefGoogle Scholar
Serôdio, J., Cruz, S., Vieira, S. and Coelho, H. (2006b) Rapid light-response curves of chlorophyll fluorescence in microalgae: relationship to steady-state light curves and non-photochemical quenching in benthic diatom-dominated assemblages. Photosynthesis Research 90, 29–43.CrossRefGoogle ScholarPubMed
Serôdio, J., Vieira, S. and Cruz, S. (2008) Photosynthetic activity, photoprotection and photoinhibition in intertidal microphytobenthos as studied in situ using variable chlorophyll fluorescence. Continental Shelf Research 28, 1363–1375.CrossRefGoogle Scholar
Shannon, T., Hatch, W.I. and Fitt, W.K. (2009) Evidence of photosynthate translocation in an algal–acoel symbiotic system: an in vivo, qualitative approach. Journal of Experimental Marine Biology and Ecology 382, 69–75.CrossRefGoogle Scholar
Sharon, Y. and Beer, S. (2008) Diurnal movements of chloroplasts in Halophila stipulacea and their effect on PAM fluorometric measurements of photosynthetic rates. Aquatic Botany 88, 273–276.CrossRefGoogle Scholar
Silva, J. and Santos, R. (2003) Daily variation patterns in seagrass photosynthesis along a vertical gradient. Marine Ecology Progress Series 257, 37–44.CrossRefGoogle Scholar
Taylor, D.L. (1974) Nutrition of algal in invertebrate symbiosis. I. Utilization of soluble organic nutrients by symbiont-free hosts. Proceedings of the Royal Society of London (Series B) 186, 357–368.Google ScholarPubMed
Thimijan, R.W. and Heins, R.D. (1983) Photometric, radiometric, and quantum light units of measure: a review of procedures for interconversion. Hortscience 18, 818–822.CrossRefGoogle Scholar
Trench, R.K. (1993) Microalgal–invertebrate symbioses: a review. Endocytobiosis and Cell Research 9, 135–175.Google Scholar
Venn, A.A, Loram, J.E. and Douglas, A.E. (2008) Photosynthetic symbiosis in animals. Journal of Experimental Botany 59, 1069–1080.CrossRefGoogle ScholarPubMed
Vieira, S., Calado, R., Coelho, H. and Serôdio, J. (2009) Effects of light exposure on the retention of kleptoplastic photosynthetic activity in the sacoglossan mollusc Elysia viridis. Marine Biology 156, 1007–1020.CrossRefGoogle Scholar
Wägele, H. and Johnsen, G. (2001) Observations on the histology and photosynthetic performance of ‘solar-powered’ opisthobranchs (Mollusca, Gastropoda, Opisthobranchia) containing symbiotic chloroplasts or zooxanthellae. Organisms Diversity and Evolution 1, 193–210.CrossRefGoogle Scholar
Warner, M.E., Fitt, W.K. and Schmidt, G.W. (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant, Cell and Environment 19, 291–299.CrossRefGoogle Scholar
White, A.J. and Critchley, C. (1999) Rapid light curves: a new fluorescence method to assess the state of the photosynthetic apparatus. Photosynthesis Research 59, 63–72.CrossRefGoogle Scholar