in

In vivo assessment of mitochondrial respiratory alternative oxidase activity and cyclic electron flow around photosystem I on small coral fragments

  • 1.

    Falkowski, P. G., Dubinsky, Z., Muscatine, L. & Porter, J. W. Light and the bioenergetics of a symbiotic coral. Bioscience 34, 705–709 (1984).

    CAS  Article  Google Scholar 

  • 2.

    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).

    CAS  PubMed  Article  Google Scholar 

  • 3.

    LaJeunesse, T. C. et al. Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570-2580.e6 (2018).

    CAS  PubMed  Article  Google Scholar 

  • 4.

    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).

    ADS  Article  Google Scholar 

  • 5.

    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).

    ADS  CAS  Google Scholar 

  • 6.

    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).

    Google Scholar 

  • 7.

    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).

    ADS  CAS  Article  Google Scholar 

  • 8.

    Wangpraseurt, D. et al. Spectral effects on Symbiodinium photobiology studied with a programmable light engine. PLoS ONE 9, e112809 (2014).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 9.

    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).

    ADS  Article  Google Scholar 

  • 10.

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 11.

    Houlbrèque, F. & Ferrier-Pagès, C. Heterotrophy in tropical scleractinian corals. Biol. Rev. 84, 1–17 (2009).

    PubMed  Article  Google Scholar 

  • 12.

    Holcomb, M., Tambutté, E., Allemand, D. & Tambutté, S. Light enhanced calcification in Stylophora pistillata: effects of glucose, glycerol and oxygen. PeerJ 2, e375 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 13.

    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).

    CAS  Article  Google Scholar 

  • 14.

    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).

    ADS  Article  Google Scholar 

  • 15.

    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).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 16.

    Blackstone, N. Mitochondria and the redox control of development in cnidarians. Semin. Cell Dev. Biol. 20, 330–336 (2009).

    CAS  PubMed  Article  Google Scholar 

  • 17.

    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).

    CAS  PubMed  Article  Google Scholar 

  • 18.

    McDonald, A. E. & Gospodaryov, D. V. Alternative NAD(P)H dehydrogenase and alternative oxidase: proposed physiological roles in animals. Mitochondrion 45, 7–17 (2019).

    CAS  PubMed  Article  Google Scholar 

  • 19.

    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).

    CAS  Article  Google Scholar 

  • 20.

    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).

    ADS  Article  Google Scholar 

  • 21.

    Nelson, H. R. & Altieri, A. H. Oxygen: The universal currency on coral reefs. Coral Reefs 38, 177–189 (2019).

    ADS  Article  Google Scholar 

  • 22.

    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).

    CAS  Article  Google Scholar 

  • 23.

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 24.

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 25.

    Raven, J. A., Suggett, D. J. & Giordano, M. Inorganic carbon concentrating mechanisms in free-living and symbiotic dinoflagellates and chromerids. J. Phycol. https://doi.org/10.1111/jpy.13050 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  • 26.

    Barott, K. L. et al. Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis. Proc. Natl. Acad. Sci. USA 112, 607–612 (2015).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 27.

    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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 28.

    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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 29.

    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).

    PubMed  Article  PubMed Central  Google Scholar 

  • 30.

    Roth, M. S. The engine of the reef: photobiology of the coral-algal symbiosis. Front. Microbiol. 5, 1–22 (2014).

    ADS  Article  Google Scholar 

  • 31.

    Roberty, S., Béraud, E., Grover, R. & Ferrier-Pagès, C. Coral productivity is co-limited by bicarbonate and ammonium availability. Microorganisms 8, 640 (2020).

    PubMed Central  Article  PubMed  Google Scholar 

  • 32.

    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).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 33.

    Cardol, P., Forti, G. & Finazzi, G. Regulation of electron transport in microalgae. Biochim. Biophys. Acta 1807, 912–918 (2011).

    CAS  PubMed  Article  Google Scholar 

  • 34.

    Papageorgiou, G. C. Chlorophyll a Fluorescence. A Signature of Photosynthesis (Springer, Dordrecht, 2004).

    Google Scholar 

  • 35.

    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).

    ADS  Article  Google Scholar 

  • 36.

    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).

    CAS  Article  Google Scholar 

  • 37.

    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).

    CAS  PubMed  Article  Google Scholar 

  • 38.

    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).

    Article  Google Scholar 

  • 39.

    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).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 40.

    Szabó, M. et al. Non-intrusive assessment of photosystem II and photosystem I in whole coral tissues. Front. Mar. Sci. 4, 269 (2017).

    Article  Google Scholar 

  • 41.

    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).

    ADS  Article  Google Scholar 

  • 42.

    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).

    CAS  PubMed  Article  Google Scholar 

  • 43.

    Maxwell, K. & Johnson, G. N. Chlorophyll fluorescence-a practical guide. J. Exp. Bot. 51, 659–668 (2000).

    CAS  PubMed  Article  Google Scholar 

  • 44.

    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).

    CAS  Article  Google Scholar 

  • 45.

    Schreiber, U. Redox changes of ferredoxin, P700, and plastocyanin measured simultaneously in intact leaves. Photosynth. Res. 134, 343–360 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 46.

    Joliot, P. & Joliot, A. Quantification of cyclic and linear flows in plants. Proc. Natl. Acad. Sci. USA 102, 4913–4918 (2005).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 47.

    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).

    CAS  PubMed  Article  Google Scholar 

  • 48.

    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).

    CAS  Article  Google Scholar 

  • 49.

    Bailleul, B., Cardol, P., Breyton, C. & Finazzi, G. Electrochromism: A useful probe to study algal photosynthesis. Photosynth. Res. 106, 179–189 (2010).

    CAS  PubMed  Article  Google Scholar 

  • 50.

    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).

    Google Scholar 

  • 51.

    Ritchie, R. J. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth. Res. 89, 27–41 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 52.

    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).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 53.

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 54.

    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).

    Article  Google Scholar 

  • 55.

    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).

    CAS  Article  Google Scholar 

  • 56.

    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).

    ADS  Article  Google Scholar 

  • 57.

    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).

    PubMed  Article  Google Scholar 

  • 58.

    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).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 59.

    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).

    CAS  PubMed  Article  Google Scholar 

  • 60.

    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).

    CAS  Google Scholar 

  • 61.

    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).

    Article  Google Scholar 

  • 62.

    Mass, T. et al. Photoacclimation of Stylophora pistillata to light extremes: metabolism and calcification. Mar. Ecol. Prog. Ser. 334, 93–102 (2007).

    ADS  CAS  Article  Google Scholar 

  • 63.

    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).

    Article  Google Scholar 

  • 64.

    Peltier, G., Tolleter, D., Billon, E. & Cournac, L. Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth. Res. 106, 19–31 (2010).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 65.

    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. https://doi.org/10.1111/nph.16738 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  • 66.

    Bailleul, B. et al. Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 524, 366–369 (2015).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 67.

    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).

    CAS  Article  Google Scholar 

  • 68.

    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).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 69.

    Szabó, M. et al. Effective light absorption and absolute electron transport rates in the coral Pocillopora damicornis. Plant Physiol. Biochem. 83, 159–167 (2014).

    ADS  PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 70.

    Kato, H. et al. Characterization of a giant photosystem I supercomplex in the symbiotic dinoflagellate Symbiodiniaceae. Plant Physiol. https://doi.org/10.1104/pp.20.00726 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  • 71.

    Alric, J. Cyclic electron flow around photosystem I in unicellular green algae. Photosynth. Res. 106, 47–56 (2010).

    CAS  PubMed  Article  Google Scholar 

  • 72.

    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).

    ADS  CAS  PubMed  Article  Google Scholar 


  • Source: Ecology - nature.com

    MIT.nano receives LEED Platinum certification

    Benthic ecosystem cascade effects in Antarctica using Bayesian network inference