Vega de Luna_2020_In vivo assessment of mitochondrial respiratory alternative oxidase activity and cyclic electron flow around photosystem I on small coral fragments.pdf
[en] The mutualistic relationship existing between scleractinian corals and their photosynthetic endosymbionts involves a complex integration of the metabolic pathways within the holobiont. Respiration and photosynthesis are the most important of these processes and although they have been extensively studied, our understanding of their interactions and regulatory mechanisms is still limited. In this work we performed chlorophyll-a fluorescence, oxygen exchange and time-resolved absorption spectroscopy measurements on small and thin fragments (0.3 cm2) of the coral Stylophora pistillata. We showed that the capacity of mitochondrial alternative oxidase accounted for ca. 25% of total coral respiration, and that the high-light dependent oxygen uptake, commonly present in isolated Symbiodiniaceae, was negligible. The ratio between photosystem I (PSI) and photosystem II (PSII) active centers as well as their respective electron transport rates, indicated that PSI cyclic electron flow occurred in high light in S. pistillata and in some branching and lamellar coral species freshly collected in the field. Altogether, these results show the potential of applying advanced biophysical and spectroscopic methods on small coral fragments to understand the complex mechanisms of coral photosynthesis and respiration and their responses to environmental changes.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Vega de Luna, Felix ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
Córdoba-Granados, Juan José
Dang, Kieu-Van
Roberty, Stéphane ✱; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecophysiologie et physiologie animale
Cardol, Pierre ✱; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues
✱ These authors have contributed equally to this work.
Language :
English
Title :
In vivo assessment of mitochondrial respiratory alternative oxidase activity and cyclic electron flow around photosystem I on small coral fragments
H2020 - 682580 - BEAL - Bioenergetics in microalgae : regulation modes of mitochondrial respiration, photosynthesis, and fermentative pathways, and their interactions in secondary algae
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique ERC - European Research Council EC - European Commission
Falkowski, P. G., Dubinsky, Z., Muscatine, L. & Porter, J. W. Light and the bioenergetics of a symbiotic coral. Bioscience 34, 705–709 (1984). DOI: 10.2307/1309663
Morris, L. A., Voolstra, C. R., Quigley, K. M., Bourne, D. G. & Bay, L. K. Nutrient availability and metabolism affect the stability of coral–symbiodiniaceae symbioses. Trends Microbiol. 27, 678–689 (2019). DOI: 10.1016/j.tim.2019.03.004
LaJeunesse, T. C. et al. Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570-2580.e6 (2018). DOI: 10.1016/j.cub.2018.07.008
Cunning, R., Silverstein, R. N. & Baker, A. C. Symbiont shuffling linked to differential photochemical dynamics of Symbiodinium in three Caribbean reef corals. Coral Reefs 37, 145–152 (2018). DOI: 10.1007/s00338-017-1640-3
Muscatine, L., Falkowski, P. G., Porter, J. W. & Dubinsky, Z. Fate of photosynthetic fixed carbon in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc. R. Soc. B Biol. Sci. 222, 181–202 (1984).
Porter, J. W. Primary productivity in the sea: Reef corals in situ. In Primary Productivity in the Sea. Environmental Science Research (ed. Falkowski, P. G.) 403–410 (Springer, Boston, 1980). DOI: 10.1007/978-1-4684-3890-1_22
Patterson, M. R., Sebens, K. P. & Olson, R. O. In situ measurements of flow effects on primary production and dark respiration in reef corals. Limnol. Oceanogr. 36, 936–948 (1991). DOI: 10.4319/lo.1991.36.5.0936
Wangpraseurt, D. et al. Spectral effects on Symbiodinium photobiology studied with a programmable light engine. PLoS ONE 9, e112809 (2014). DOI: 10.1371/journal.pone.0112809
Kühl, M. et al. Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar. Ecol. Prog. Ser. 117, 159–172 (1995). DOI: 10.3354/meps117159
Burriesci, M. S., Raab, T. K. & Pringle, J. R. Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J. Exp. Biol. 215, 3467–3477 (2012). DOI: 10.1242/jeb.070946
Houlbrèque, F. & Ferrier-Pagès, C. Heterotrophy in tropical scleractinian corals. Biol. Rev. 84, 1–17 (2009). DOI: 10.1111/j.1469-185X.2008.00058.x
Holcomb, M., Tambutté, E., Allemand, D. & Tambutté, S. Light enhanced calcification in Stylophora pistillata: effects of glucose, glycerol and oxygen. PeerJ 2, e375 (2014). DOI: 10.7717/peerj.375
Agostini, S., Fujimura, H., Hayashi, H. & Fujita, K. Mitochondrial electron transport activity and metabolism of experimentally bleached hermatypic corals. J. Exp. Mar. Biol. Ecol. 475, 100–107 (2016). DOI: 10.1016/j.jembe.2015.11.012
Imbs, A. B. & Yakovleva, I. M. Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress: and experimental approach. Coral Reefs 31, 31–41 (2012). DOI: 10.1007/s00338-011-0817-4
Dunn, S. R., Pernice, M., Green, K., Hoegh-Guldberg, O. & Dove, S. G. Thermal stress promotes host mitochondrial degradation in symbiotic cnidarians: are the batteries of the reef going to run out?. PLoS ONE 7, e39024 (2012). DOI: 10.1371/journal.pone.0039024
Blackstone, N. Mitochondria and the redox control of development in cnidarians. Semin. Cell Dev. Biol. 20, 330–336 (2009). DOI: 10.1016/j.semcdb.2008.12.006
McDonald, A. E., Vanlerberghe, G. C. & Staples, J. F. Alternative oxidase in animals: unique characteristics and taxonomic distribution. J. Exp. Biol. 212, 2627–2634 (2009). DOI: 10.1242/jeb.032151
McDonald, A. E. & Gospodaryov, D. V. Alternative NAD(P)H dehydrogenase and alternative oxidase: proposed physiological roles in animals. Mitochondrion 45, 7–17 (2019). DOI: 10.1016/j.mito.2018.01.009
Raven, J. A. & Beardall, J. Consequences of the genotypic loss of mitochondrial Complex I in dinoflagellates and of phenotypic regulation of Complex I content in other photosynthetic organisms. J. Exp. Bot. 68, 2683–2692 (2017). DOI: 10.1093/jxb/erx149
Oakley, C. A., Hopkinson, B. M. & Schmidt, G. W. Mitochondrial terminal alternative oxidase and its enhancement by thermal stress in the coral symbiont Symbiodinium. Coral Reefs 33, 543–552 (2014). DOI: 10.1007/s00338-014-1147-0
Nelson, H. R. & Altieri, A. H. Oxygen: The universal currency on coral reefs. Coral Reefs 38, 177–189 (2019). DOI: 10.1007/s00338-019-01765-0
Iglesias-prieto, A. R., Govind, N. S. & Trench, R. K. Isolation and characterization of three membrane bound chlorophyll-protein complexes from four dinoflagellate species. Philos. Trans. R. Soc. Lond. B 340, 381–392 (1993). DOI: 10.1098/rstb.1993.0080
Aihara, Y., Takahashi, S. & Minagawa, J. Heat induction of cyclic electron flow around photosystem I in the symbiotic dinoflagellate Symbiodinium. Plant Physiol. 171, 522–529 (2016). DOI: 10.1104/pp.15.01886
Leggat, W., Badger, M. & Yellowlees, D. Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol. 121, 1247–1255 (1999). DOI: 10.1104/pp.121.4.1247
Raven, J. A., Suggett, D. J. & Giordano, M. Inorganic carbon concentrating mechanisms in free-living and symbiotic dinoflagellates and chromerids. J. Phycol. 10.1111/jpy.13050 (2020). DOI: 10.1111/jpy.13050
Barott, K. L. et al. Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis. Proc. Natl. Acad. Sci. USA 112, 607–612 (2015). DOI: 10.1073/pnas.1413483112
Mayfield, A. B., Hsiao, Y. Y., Chen, H. K. & Chen, C. S. Rubisco expression in the dinoflagellate Symbiodinium sp. is influenced by both photoperiod and endosymbiotic lifestyle. Mar. Biotechnol. 16, 371–384 (2014). DOI: 10.1007/s10126-014-9558-z
Tremblay, P., Grover, R., Maguer, J. F., Legendre, L. & Ferrier-Pagès, C. Autotrophic carbon budget in coral tissue: A new 13C-based model of photosynthate translocation. J. Exp. Biol. 215, 1384–1393 (2012). DOI: 10.1242/jeb.065201
Maor-Landaw, K., van Oppen, M. J. H. & McFadden, G. I. Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae). Ecol. Evol. 10, 451–466 (2020). DOI: 10.1002/ece3.5910
Roth, M. S. The engine of the reef: photobiology of the coral-algal symbiosis. Front. Microbiol. 5, 1–22 (2014). DOI: 10.3389/fmicb.2014.00422
Roberty, S., Béraud, E., Grover, R. & Ferrier-Pagès, C. Coral productivity is co-limited by bicarbonate and ammonium availability. Microorganisms 8, 640 (2020). DOI: 10.3390/microorganisms8050640
Tchernov, D. et al. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc. Natl. Acad. Sci. USA 101, 13531–13535 (2004). DOI: 10.1073/pnas.0402907101
Cardol, P., Forti, G. & Finazzi, G. Regulation of electron transport in microalgae. Biochim. Biophys. Acta 1807, 912–918 (2011). DOI: 10.1016/j.bbabio.2010.12.004
Papageorgiou, G. C. Chlorophyll a Fluorescence. A Signature of Photosynthesis (Springer, Dordrecht, 2004). DOI: 10.1007/978-1-4020-3218-9
Hennige, S. J., Suggett, D. J., Warner, M. E., McDougall, K. E. & Smith, D. J. Photobiology of Symbiodinium revisited: Bio-physical and bio-optical signatures. Coral Reefs 28, 179–195 (2009). DOI: 10.1007/s00338-008-0444-x
Reynolds, J. M. C., Bruns, B. U., Fitt, W. K. & Schmidt, G. W. Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc. Natl. Acad. Sci. USA 105, 17206 (2008). DOI: 10.1073/pnas.0805187105
Roberty, S., Bailleul, B., Berne, N., Franck, F. & Cardol, P. PSI Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp., symbiotic dinoflagellates of cnidarians. New Phytol. 204, 81–91 (2014). DOI: 10.1111/nph.12903
Dang, K. V., Pierangelini, M., Roberty, S. & Cardol, P. Alternative photosynthetic electron transfers and bleaching phenotypes upon acute heat stress in Symbiodinium and Breviolum spp. (Symbiodiniaceae) in culture. Front. Mar. Sci. 6, 1–10 (2019). DOI: 10.3389/fmars.2019.00656
Hoogenboom, M. O., Campbell, D. A., Beraud, E., DeZeeuw, K. & Ferrier-Pagès, C. Effects of light, food availability and temperature stress on the function of photosystem II and photosystem I of coral symbionts. PLoS ONE 7, e30167 (2012). DOI: 10.1371/journal.pone.0030167
Szabó, M. et al. Non-intrusive assessment of photosystem II and photosystem I in whole coral tissues. Front. Mar. Sci. 4, 269 (2017). DOI: 10.3389/fmars.2017.00269
Enríquez, S., Méndez, E. R. & Iglesias-Prieto, R. Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol. Oceanogr. 50, 1025–1032 (2005). DOI: 10.4319/lo.2005.50.4.1025
Gilmore, A. M. et al. Simultaneous time resolution of the emission spectra of fluorescent proteins and zooxanthellar chlorophyll in reef-building corals. Photochem. Photobiol. 77, 515 (2003). DOI: 10.1562/0031-8655(2003)077<0515:STROTE>2.0.CO;2
Maxwell, K. & Johnson, G. N. Chlorophyll fluorescence-a practical guide. J. Exp. Bot. 51, 659–668 (2000). DOI: 10.1093/jexbot/51.345.659
Sandmann, G., Reck, H., Kessler, E. & Böger, P. Distribution of plastocyanin and soluble plastidic cytochrome c in various classes of algae. Arch. Microbiol. 134, 23–27 (1983). DOI: 10.1007/BF00429401
Schreiber, U. Redox changes of ferredoxin, P700, and plastocyanin measured simultaneously in intact leaves. Photosynth. Res. 134, 343–360 (2017). DOI: 10.1007/s11120-017-0394-7
Joliot, P. & Joliot, A. Quantification of cyclic and linear flows in plants. Proc. Natl. Acad. Sci. USA 102, 4913–4918 (2005). DOI: 10.1073/pnas.0501268102
Witt, H. et al. Species-specific differences of the spectroscopic properties of P700: Analysis of the influence of non-conserved amino acid residues by site-directed mutagenesis of photosystem I from Chlamydomonas reinhardtii. J. Biol. Chem. 278, 46760–46771 (2003). DOI: 10.1074/jbc.M304776200
Klughammer, C. & Schreiber, U. An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192, 261–268 (1994). DOI: 10.1007/BF01089043
Bailleul, B., Cardol, P., Breyton, C. & Finazzi, G. Electrochromism: A useful probe to study algal photosynthesis. Photosynth. Res. 106, 179–189 (2010). DOI: 10.1007/s11120-010-9579-z
Vega De Luna, F., Dang, K. V., Cardol, M., Roberty, S. & Cardol, P. Photosynthetic capacity of the endosymbiotic dinoflagellate Cladocopium sp. is preserved during digestion of its jellyfish host Mastigias papua by the anemone Entacmaea medusivora. FEMS Microbiol. Ecol. 95, 1–7 (2019).
Ritchie, R. J. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth. Res. 89, 27–41 (2006). DOI: 10.1007/s11120-006-9065-9
Hume, B. C. C. et al. An improved primer set and amplification protocol with increased specificity and sensitivity targeting the Symbiodinium ITS2 region. PeerJ 6, e4816 (2018). DOI: 10.7717/peerj.4816
Hume, B. C. C. et al. SymPortal: A novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol. Ecol. Resour. 19, 1063–1080 (2019). DOI: 10.1111/1755-0998.13004
Shafir, S., Van Rijn, J. & Rinkevich, B. Nubbing of coral colonies: a novel approach for the development of inland broodstocks. Aquar. Sci. Conserv. 3, 183–190 (2001). DOI: 10.1023/A:1011364732176
Hoadley, K. D. et al. Host–symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. Sci. Rep. 9, 1–15 (2019). DOI: 10.1038/s41598-019-46412-4
Heyward, A. J. & Collins, J. D. Fragmentation in Montipora ramosa: the genet and ramet concept applied to a reef coral. Coral Reefs 4, 35–40 (1985). DOI: 10.1007/BF00302202
Raz-Bahat, M., Erez, J. & Rinkevich, B. In vivo light-microscopic documentation for primary calcification processes in the hermatypic coral Stylophora pistillata. Cell Tissue Res. 325, 361–368 (2006). DOI: 10.1007/s00441-006-0182-8
Warner, M. E., Fitt, W. K. & Schmidt, G. W. Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc. Natl. Acad. Sci. USA 96, 8007–8012 (1999). DOI: 10.1073/pnas.96.14.8007
Rehman, A. U. et al. Symbiodinium sp. cells produce light-induced intra- and extracellular singlet oxygen, which mediates photodamage of the photosynthetic apparatus and has the potential to interact with the animal host in coral symbiosis. New Phytol. 212, 472–484 (2016). DOI: 10.1111/nph.14056
Hill, R. & Ralph, P. J. Dark-induced reduction of the plastoquinone pool in zooxanthellae of scleractinian corals and implications for measurements of chlorophyll a fluorescence. Symbiosis 46, 45–56 (2008).
Einbinder, S. et al. Novel adaptive photosynthetic characteristics of mesophotic symbiotic microalgae within the reef-building coral, Stylophora pistillata. Front. Mar. Sci. 3, 1–9 (2016). DOI: 10.3389/fmars.2016.00195
Mass, T. et al. Photoacclimation of Stylophora pistillata to light extremes: metabolism and calcification. Mar. Ecol. Prog. Ser. 334, 93–102 (2007). DOI: 10.3354/meps334093
Ferrier-Pagès, C., Gattuso, J. P., Dallot, S. & Jaubert, J. Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellae coral Stylophora pistillata. Coral Reefs 19, 103–113 (2000). DOI: 10.1007/s003380000078
Peltier, G., Tolleter, D., Billon, E. & Cournac, L. Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth. Res. 106, 19–31 (2010). DOI: 10.1007/s11120-010-9575-3
Pierangelini, M., Thiry, M. & Cardol, P. Different levels of energetic coupling between photosynthesis and respiration do not determine the occurrence of adaptive responses of Symbiodiniaceae to global warming. New Phytol. 10.1111/nph.16738 (2020). DOI: 10.1111/nph.16738
Bailleul, B. et al. Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 524, 366–369 (2015). DOI: 10.1038/nature14599
Badger, M. R. et al. Electron flow to oxygen in higher plants and algae: Rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philos. Trans. R. Soc. B 355, 1433–1446 (2000). DOI: 10.1098/rstb.2000.0704
Fan, D. Y. et al. Obstacles in the quantification of the cyclic electron flux around photosystem I in leaves of C3 plants. Photosynth. Res. 129, 239–251 (2016). DOI: 10.1007/s11120-016-0223-4
Szabó, M. et al. Effective light absorption and absolute electron transport rates in the coral Pocillopora damicornis. Plant Physiol. Biochem. 83, 159–167 (2014). DOI: 10.1016/j.plaphy.2014.07.015
Kato, H. et al. Characterization of a giant photosystem I supercomplex in the symbiotic dinoflagellate Symbiodiniaceae. Plant Physiol. 10.1104/pp.20.00726 (2020). DOI: 10.1104/pp.20.00726
Alric, J. Cyclic electron flow around photosystem I in unicellular green algae. Photosynth. Res. 106, 47–56 (2010). DOI: 10.1007/s11120-010-9566-4
Melis, A. & Jeanette, J. S. Stoichiometry of system I and system II reaction centers and of plastoquinone in different photosynthetic membranes. Proc. Natl. Acad. Sci. USA. 77, 4712–4716 (1980). DOI: 10.1073/pnas.77.8.4712
