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3 - …And Nothing Was the Same Anymore: The Rise in O2 and Consequences for Photoautotrophs

from Part I - Origins and Consequences of Early Photosynthetic Organisms

Published online by Cambridge University Press:  24 October 2024

Mario Giordano
Affiliation:
Università degli Studi di Ancona, Italy
John Beardall
Affiliation:
Monash University, Victoria
John A. Raven
Affiliation:
University of Dundee
Stephen C. Maberly
Affiliation:
UK Centre for Ecology & Hydrology, Lancaster
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Summary

The evolution of oxygenic photosynthesis had profound effects on the biogeochemistry of the planet. The increase in atmospheric oxygen levels brought about alterations to a range of biogeochemical processes involving changes in the availability of a host of elements, including nitrogen, sulfur and many metal ions such as iron and manganese, central to biological activities. Critically for photosynthetic organisms, the increase in oxygen levels in the atmosphere following the evolution of oxygenic photosynthesis and the Great Oxidation Event had consequences for the assimilation of inorganic carbon via the enzyme ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco). Although there are a number of alternative pathways leading to autotrophic CO2 assimilation, 99% of primary productivity on the planet is carried out by processes that involve Rubisco and the Benson–Calvin–Bassham cycle. The accumulation of O2 in the atmosphere also had major repercussions for increasing the energetic yield of the catabolism of photosynthate by allowing oxidative respiration, with a much greater ATP yield than from anaerobic fermentative processes. The interaction of O2 with UVC radiation led to the production of UVC- and UVB-absorbing O3. This also significantly influenced life on Earth and facilitated the colonisation of the upper ocean and terrestrial surface.

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Publisher: Cambridge University Press
Print publication year: 2024

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References

Amoroso, G., Sültemeyer, D. F., Thyssen, C. et al. (1998). Uptake of HCO3 and CO2 in cells and chloroplasts from the microalgae Chlamydomonas reinhardtii and Dunaliella tertiolecta. Plant Physiology 116: 193201.CrossRefGoogle Scholar
Anbar, A. D. & Knoll, A. H. (2002). Proterozoic ocean chemistry and evolution: A bioinorganic bridge? Science 297: 11371142.CrossRefGoogle ScholarPubMed
Anderson, L. E. (1971). Chloroplast and cytoplasmic enzymes. II. Pea leaf triose phosphate isomerases. Biochimica et Biophysica Acta 235: 237–44.Google ScholarPubMed
Aono, R., Sato, T., Imanaka, T. et al. (2015). A pentose bisphosphate pathway for nucleoside degradation in Archaea. Nature Chemical Biology 11: 355–360.CrossRefGoogle ScholarPubMed
Aubry, S., Brown, N. J. & Hibberd, J. M. (2011). The role of proteins in C3 plants prior to their recruitment into the C4 pathway. Journal of Experimental Botany 62: 30493059.CrossRefGoogle Scholar
Badger, M. R., Andrews, T. J., Whitney, S. M. et al. (1998). The diversity and coevolution of Rubiscos, plastids, pyrenoids and chloroplast-based CO2-concentrating mechanisms in algae. Canadian Journal of Botany 76: 10521071.CrossRefGoogle Scholar
Badger, M. R., Hanson, D. T. & Price, G. D. (2002). Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Functional Plant Biology 29: 407416.CrossRefGoogle ScholarPubMed
Bathellier, C., Tcherkez, G., Lorimer, G. H. et al. (2018). Rubisco is not really so bad. Plant, Cell & Environment 41: 705716.CrossRefGoogle Scholar
Beardall, J. & Raven, J. A. (2020). Structural and biochemical features of carbon acquisition in algae. In: Larkum, A. W. D., Grossman, A. & Raven, J. A. (eds.) Photosynthesis in Algae: Biochemical and Physiological Mechanisms. Advances in Photosynthesis and Respiration, Vol. 45. Springer, Cham, pp. 141160. https://doi.org/10.1007/978-3-030-33397-3_7.CrossRefGoogle Scholar
Beardall, J., Mukerji, D., Glover, H. E. et al. (1976). The path of carbon in photosynthesis by marine phytoplankton. Journal of Phycology 12: 409417.CrossRefGoogle Scholar
Bhatti, S. & Colman, B. (2008). Inorganic carbon acquisition in some synurophyte algae. Physiologia Plantarum 133: 3340.CrossRefGoogle ScholarPubMed
Blanc, G., Agarkova, I., Grimwood, J. et al. (2012). The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biology 13: R39. https://doi.org/10.1186/gb-2012–13-5-r39.CrossRefGoogle ScholarPubMed
Boller, A. J., Thomas, P. J., Cavenaugh, C. M. et al. (2011). Low stable isotope fractionation by coccolithophore RuBISCO. Geochimica Cosmochimica Acta 75: 72007207.CrossRefGoogle Scholar
Bonar, P. T. & Casey, J. R. (2008). Plasma membrane Cl/HCO3 exchangers: Structure, mechanism and physiology. Channels 2: 337345.CrossRefGoogle ScholarPubMed
Borkhsenious, O. N., Mason, C. B. & Moroney, J. V. (1998). The intracellular localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in Chlamydomonas reinhardtii. Plant Physiology 116: 15851591.CrossRefGoogle ScholarPubMed
Bowes, G., Ogren, W. L. & Hageman, R. H. (1971). Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. Biochemical and Biophysical Research Communications 45: 716722.CrossRefGoogle ScholarPubMed
Bowes, G. (2011). Single-cell C4 photosynthesis in aquatic plants. In: Raghevendra, A. S. & Sage, R. (eds.) C4 Photosynthesis and Related CO2 Concentrating Mechanisms. Springer, Berlin, pp. 6380.Google Scholar
Bowes, G., Holaday, A. S., Van, T. K. et al. (1978). Photosynthetic and photorespiratory carbon metabolism in aquatic plants. In: Hall, D. O., Coombs, J. & Goodwin, T. W. (eds.) Photosynthesis 77, Proceedings of the Fourth International Congress on Photosynthesis. The Biochemical Society, London, pp. 289298.Google Scholar
Bowes, G., Rao, S. K., Estavillo, G. M. et al. (2002). C4 mechanisms in aquatic angiosperms: A comparison with terrestrial C4 systems. Functional Plant Biology 29: 379392.CrossRefGoogle ScholarPubMed
Burkhardt, S., Amoroso, G., Riebesell, U. et al. (2001). CO2 and HCO3 uptake in marine diatoms acclimated to different CO2 concentrations. Limnology and Oceanography 46: 13781391.CrossRefGoogle Scholar
Campbell, W. J. & Ogren, W. L. (1990). Glyoxylate inhibition of ribulose bisphosphate carboxylase/oxygenase activation in intact, lysed, and reconstituted chloroplasts. Photosynthesis Research 23: 257. https://doi.org/10.1007/BF00034856.CrossRefGoogle ScholarPubMed
Canfield, D. E. (2004). The evolution of the Earth surface sulfur reservoir. American Journal of Science 304: 839861.CrossRefGoogle Scholar
Chi, S., Wu, S., Yu, J. et al. (2014). Phylogeny of C4-photosynthesis genes based on algal and genomic data supports an archaeal/proteobacterial origin and multiple duplications for most C4-related genes. PLOS ONE 9: e110154.CrossRefGoogle ScholarPubMed
Colman, B. & Rotatore, C. (1995). Photosynthetic inorganic carbon uptake and accumulation in two marine diatoms. Plant, Cell & Environment 18: 919924.CrossRefGoogle Scholar
Cook, C. M., Mulligan, R. M. & Tolbert, N. E. (1985). Inhibition and stimulation of ribulose-1,5-bisphosphate carboxylase-oxygenase by glyoxylate. Archives of Biochemistry and Biophysics 240: 392401.CrossRefGoogle ScholarPubMed
Dellero, Y., Jossier, M., Glab, N. et al. (2016). Decreased glycolate oxidase activity leads to altered carbon allocation and leaf senescence after a transfer from high CO2 to ambient air in Arabidopsis thaliana. Journal of Experimental Botany 67: 3149–63.CrossRefGoogle ScholarPubMed
DiMario, R. J., Machingura, M. C., Waldrop, G. L. et al. (2017). The many types of carbonic anhydrases in photosynthetic organisms. Plant Science 268: 1117.CrossRefGoogle ScholarPubMed
Dodge, J. D. (1973). The Fine Structure of Algal Cells. Academic Press, London, p 261.Google Scholar
Eisenhut, M., Ruth, W., Haimovitch, M. et al. (2008). The photorespiratory glycolate metabolism is essential for cyanobacteria and may have been conveyed endosymbiotically to plants. Proceedings of the National Academy of Sciences USA 105: 1719917204.CrossRefGoogle Scholar
Flynn, K. J., Blackford, J. C., Baird, M. E. et al. (2012). Changes in pH at the exterior surface of plankton with ocean acidification. Nature Climate Change 2: 510513.CrossRefGoogle Scholar
Frolov, E. N., Kublanov, I. V., Toshchakov, S. V. et al. (2019). Form III RubisCO-mediated transaldolase variant of the Calvin cycle in a chemolithoautotrophic bacterium. Proceedings of the National Academy of Sciences USA 116(37): 1863818646.CrossRefGoogle Scholar
Fukuzawa, H., Miura, K., Ishizaki, K. et al. (2001). Ccm1, a regulatory gene controlling the induction of a carbon concentrating mechanism in Chlamydomonas reinhardtii by sensing CO2 availability. Proceedings of the National Academy of Sciences USA 98: 53475352.CrossRefGoogle ScholarPubMed
Gee, C. W. & Niyogi, K. K. (2017). The carbonic anhydrase CAH1 is an essential component of the carbon-concentrating mechanism of Nannochloropsis oceanica. Proceedings of the National Academy of Sciences USA 114: 45374547.CrossRefGoogle ScholarPubMed
Gill, B. C., Lyons, T. W. & Saltzman, M. R. (2007). Parallel, high resolution carbon and sulfur isotope records of the evolving Palaeozoic marine sulfur reservoir. Palaeogeography, Palaeoclimatology, Palaoecology 256: 156173.CrossRefGoogle Scholar
Gill, B. C., Lyons, T. W. & Jenkyns, H. C. (2011). A global perturbation to the sulfur cycle during the Toarcian Ocean Anoxic Event. Earth and Planetary Science Letters 312: 484496.CrossRefGoogle Scholar
Giordano, M. & Raven, J. A. (2014). Nitrogen and sulfur assimilation in plants and algae. Aquatic Botany 118: 4561.CrossRefGoogle Scholar
Giordano, M., Beardall, J. & Raven, J. A. (2005a). CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology 6: 99131.CrossRefGoogle Scholar
Giordano, M., Norici, A. & Hell, R. (2005b). Sulfur and phytoplankton: Acquisition, metabolism and impact on the environment. New Phytologist 166(2), 371382.CrossRefGoogle ScholarPubMed
Giordano, M., Pezzoni, V. & Hell, R. (2000). Strategies for the allocation of resources under sulfur limitation in the green alga Dunaliella salina. Plant Physiology 124, 857864.CrossRefGoogle ScholarPubMed
Holaday, A. S. & Bowes, G. (1980). C4 acid metabolism and dark CO2 fixation in a submersed aquatic macrophyte (Hydrilla verticillata). Plant Physiology 65: 331335.CrossRefGoogle Scholar
Hopkinson, B. M., Meile, C. & Shen, C. (2013). Quantification of extracellular carbonic anhydrase in two marine diatoms and investigation of its role. Plant Physiology 162: 11421152.CrossRefGoogle ScholarPubMed
Huertas, I. E., Colman, B. & Espie, G. S. (2002). Inorganic carbon acquisition and its energization in eustigmatophyte algae. Functional Plant Biology 29: 271–77.CrossRefGoogle ScholarPubMed
Janouškovec, J., Gavelis, G. S., Burki, F. et al. (2017). Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics. Proceedings of the National Academy of Sciences, USA 114(2): E171E180. https://doi.org/10.1073/pnas.1614842114.CrossRefGoogle ScholarPubMed
Janouškovec, J., Paskerova, G. G., Miroliubova, T. S. et al. (2019). Apicomplexan-like parasites are polyphyletic and widely but selectively dependent on cryptic plastid organelles. eLife 8: e49662. https://doi.org/10.7554/eLife.49662.CrossRefGoogle ScholarPubMed
John-McKay, M. & Colman, B. (1997). Variation in the occurrence of external carbonic anhydrase among strains of the marine diatom Phaeodactylum tricornutum (Bacillariophyceae). Journal of Phycology 33: 988990.CrossRefGoogle Scholar
Johnston, A. M. & Raven, J. A. (1996). Inorganic carbon accumulation by the marine diatom Phaeodactylum tricornutum. European Journal of Phycology 31: 285290.CrossRefGoogle Scholar
Johnston, A. M., Raven, J. A., Beardall, J. & Leegood, R. C. (2001). Photosynthesis in a marine diatom. Nature 412: 4041.CrossRefGoogle Scholar
Kah, L. C., Lyons, T. W. & Frank, T. D. (2004). Low marine sulphate and protracted oxygenation of the Proterozoic biosphere. Nature 431: 834838.CrossRefGoogle ScholarPubMed
Kaldenhoff, R., Kai, L. & Uehlein, N. (2014). Aquaporins and membrane diffusion of CO2 in living organisms. Biochimica et Biophysica Acta 1840: 15921595.CrossRefGoogle ScholarPubMed
Karsten, U., Kück, K., Vogt, C. et al. (1996). Dimethylsulfoniopropionate production in phototrophic organisms and its physiological functions as a cryoprotectant. In Kiene, R. P., Visscher, P. T., Keller, M. D. & Kirst, G. O., (eds.) Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds. Springer, New York, NY, pp. 143153.CrossRefGoogle Scholar
Keeley, J. E. (1998). CAM photosynthesis in submerged aquatic plants. Botanical Reviews 64: 121175. https://doi.org/10.1007/BF02856581.CrossRefGoogle Scholar
Keeley, J. E. & Rundel, P. W. (2003). Evolution of CAM and C4 carbon-concentrating mechanisms. International Journal of Plant Science 8: 683690.Google Scholar
Keller, M. D., Kiene, R. P., Matrai, P. A. et al. (1999). Production of glycine betaine and dimethylsulfoniopropionate in marine phytoplankton. II. N-limited chemostat cultures. Marine Biology 135: 249257.CrossRefGoogle Scholar
Kerfeld, C. & Melnicki, M. R. (2016). Assembly, function and evolution of cyanobacterial carboxysomes. Current Opinion in Plant Biology 31: 6675.CrossRefGoogle ScholarPubMed
Kevekordes, K., Holland, D., Jenkins, S. et al. (2006). Inorganic carbon acquisition by eight species of Caulerpa. Phycologia 45: 442449.CrossRefGoogle Scholar
Kikutani, S., Nakajima, K., Nagasato, C. et al. (2016). Thylakoid luminal θ-carbonic anhydrase critical for growth and photosynthesis in the marine diatom. Phaeodactylum tricornutum. Proceedings of the National Academy of Sciences USA 113: 98289833.CrossRefGoogle ScholarPubMed
Koch, M., Bowes, G., Ross, C. et al. (2013). Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology 19: 103132.CrossRefGoogle ScholarPubMed
Korb, R. E., Saville, P. J., Johnston, A. M. et al. (1997). Sources of inorganic carbon for photosynthesis by three species of marine diatoms. Journal of Phycology 33: 433440.CrossRefGoogle Scholar
Kroth, P. G. (2015). The biodiversity of carbon assimilation. Journal of Plant Physiology 172: 7681.CrossRefGoogle ScholarPubMed
Kübler, J. E. & Raven, J. A. (1994). Consequences of light limitation for carbon acquisition in three rhodophytes. Marine Ecology Progress Series 110: 203209.CrossRefGoogle Scholar
Kübler, J. E. & Raven, J. A. (1995). The interaction between inorganic carbon supply and light supply in Palmaria palmata (Rhodophyta). Journal of Phycology 31: 369375.CrossRefGoogle Scholar
Lapointe, M., MacKenzie, T. D. B. & Morse, D. (2008). An external δ-carbonic anhydrase in a free-living marine dinoflagellate may circumvent diffusion-limited carbon acquisition. Plant Physiology 147: 14271436.CrossRefGoogle Scholar
Larkum, A. W. D., Davey, P. A., Kuo, J. et al. (2017). Carbon-concentrating mechanisms in seagrasses. Journal of Experimental Botany 68: 37733784.CrossRefGoogle ScholarPubMed
Leggat, W., Badger, M. R. & Yellowlees, D. C. (1999). Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiology 121: 12471255.CrossRefGoogle ScholarPubMed
Lenton, T. M., Crouch, M., Johnson, M. et al. (2012). First plants cooled the Ordovician. Nature Geoscience 5: 8689.CrossRefGoogle Scholar
Maberly, S. C., Ball, L. A., Raven, J. A. et al. (2009). Inorganic carbon acquisition by chrysophytes. Journal of Phycology 45: 10571061.CrossRefGoogle ScholarPubMed
Maberly, S. C. & Madsen, T. V. (2002). Freshwater angiosperms carbon concentrating mechanisms: Processes and patterns. Functional Plant Biology 29: 393405.CrossRefGoogle ScholarPubMed
Machingura, M. C., Bajsa-Hirschel, J., Laborde, S. M. et al. (2017). Identification and characterization of a solute carrier, CIA8, involved in inorganic carbon acclimation in Chlamydomonas reinhardtii. Journal of Experimental Botany 68: 38793890.CrossRefGoogle ScholarPubMed
Mackinder, L. C. M. (2018). The Chlamydomonas CO2-concentrating mechanism and its potential for engineering photosynthesis in plants. New Phytologist 217: 5461.CrossRefGoogle ScholarPubMed
Mackinder, L., Chen, C., Leib, R. et al. (2017). A spatial interactome reveals the protein organization of the algal CO2 concentrating mechanism. Cell 171: 133147.CrossRefGoogle Scholar
Magnin, N. C., Cooley, B. A., Reiskind, J. B. et al. (1997). Regulation and localization of key enzymes during the induction of Kranz-less, C4-type photosynthesis in Hydrilla verticillata. Plant Physiology 115: 16811689.CrossRefGoogle ScholarPubMed
Matsuda, Y., Hopkinson, B. M., Nakajima, K. et al. (2017). Mechanisms of carbon dioxide acquisition and CO2 sensing in marine diatoms: A gateway to carbon metabolism. Philosophical Transactions of the Royal Society B 372: 20160403.CrossRefGoogle ScholarPubMed
McKay, R. M. L. & Gibbs, S. P. (1991). Composition and function of pyrenoids: Cytochemical and immunocytochemical approaches. Canadian Journal of Botany 69: 10401052.CrossRefGoogle Scholar
Meyer, M. T., Genkov, T., Skepper, J. N. et al. (2012). Rubisco small-subunit α-helices control pyrenoid formation in Chlamydomonas. Proceedings of the National Academy of Sciences USA 109: 1947419479.CrossRefGoogle ScholarPubMed
Meyer, M. T. & Griffiths, H. (2013). Origins and diversity of eukaryotic CO2-concentrating mechanisms: Lessons for the future. Journal of Experimental Botany 64: 769786.CrossRefGoogle ScholarPubMed
Meyer, M. T., Whittaker, C. & Griffiths, H. (2017). The algal pyrenoid: Key unanswered questions. Journal of Experimental Botany 68: 37393749.CrossRefGoogle ScholarPubMed
Mitchell, C. & Beardall, J. (1996). Inorganic carbon uptake by an Antarctic sea-ice diatom, Nitzschia frigida. Polar Biology 21: 310315.Google Scholar
Mitchell, M. C., Metodieva, G., Metodiev, M. V. et al. (2017). Pyrenoid loss impairs carbon-concentrating mechanism induction and alters primary metabolism in Chlamydomonas reinhardtii. Journal of Experimental Botany 68: 38913902.CrossRefGoogle ScholarPubMed
Morita, E., Abe, T., Tsuzuki, M. et al. (1998). Presence of the CO2-concentrating mechanism in some species of the pyrenoid-less free-living algal genus Chloromonas (Volvocales, Chlorophyta). Planta 204: 269276.CrossRefGoogle ScholarPubMed
Morita, E., Abe, T., Tsuzuki, M. et al. (1999). Role of pyrenoids in the CO2-concentrating mechanism: Comparative morphology, physiology and molecular phylogenetic analysis of closely related strains of Chlamydomonas and Chloromonas (Volvocales). Planta 208: 365372.CrossRefGoogle Scholar
Morris, I., Beardall, J. & Mukerji, D. (1978). The mechanisms of carbon fixation in phytoplankton. Mitteilungen. Internationale Vereiningung für Theoretische und Angewandte Limnologie 21: 174–83.Google Scholar
Mukherjee, A., Lau, C. S., Walker, C. E. et al. (2019). Thylakoid localized bestrophin-like proteins are essential for the CO2 concentrating mechanism of Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences USA 116: 1691516920.CrossRefGoogle ScholarPubMed
Munoz, J. & Merrett, M. J. (1989). Inorganic carbon transport in some marine eukaryotic microalgae. Planta 178: 450455.CrossRefGoogle ScholarPubMed
Nakajima, K., Tanaka, A. & Matsuda, Y. (2013). SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater. Proceedings of the National Academy of Sciences USA 110: 17671772.CrossRefGoogle Scholar
Obornik, M., Vancová, M., Lai, D.-H. et al. (2011). Morphology and ultrastructure of multiple life cycle stages of the photosynthetic relative of Apicomplexa, Chromera velia. Protist 162: 115130.CrossRefGoogle ScholarPubMed
Ogawa, T., Miyano, A. & Inoue, Y. (1985). Photosystem-I-driven inorganic carbon transport in the cyanobacterium, Anacystis nidulans. Biochimica et Biophysica Acta. 808: 7475.Google Scholar
Ogawa, T. & Ogren, W. L. (1985). Action spectra for accumulation of inorganic carbon in the cyanobacterium, Anabaena variabilis. Photochemistry and Photobiology 41: 583587.CrossRefGoogle Scholar
Ohnishi, N., Mukherjee, B., Tsujikawa, T. et al. (2010). Expression of a low CO2-inducible protein, LCI1, increases inorganic carbon uptake in the green alga Chlamydomonas reinhardtii. Plant Cell 22: 3105–311.CrossRefGoogle ScholarPubMed
Omata, T., Price, G. D., Badger, M. R. et al. (1999). Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proceedings of the National Academy of Sciences USA 96: 1357113576.CrossRefGoogle Scholar
Palmqvist, K., Sundblad, L.-G., Wingsle, G. et al. (1990). Acclimation of photosynthetic light reactions during induction of inorganic carbon accumulation in the green alga Chlamydomonas reinhardtii. Plant Physiology 94: 357–66.CrossRefGoogle ScholarPubMed
Patel, B. N. & Merrett, M. J. (1986). Regulation of carbonic anhydrase activity, inorganic carbon uptake and photosynthetic biomass yield in Chlamydomonas reinhardtii. Planta 169: 8186.CrossRefGoogle Scholar
Price, G. D., Badger, M. R., Woodger, F. J. et al. (2008). Advances in understanding the cyanobacterial CO2- concentrating-mechanism (CCM): Functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. Journal of Experimental Botany 59: 14411461.CrossRefGoogle ScholarPubMed
Price, G. D., Maeda, S., Omata, T. et al. (2002). Modes of active inorganic carbon uptake in the cyanobacterium Synechococcus sp. PCC7942. Functional Plant Biology 29: 131149.CrossRefGoogle Scholar
Price, G. D., Woodger, F. J., Badger, M. R. et al. (2004). Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proceedings of the National Academy of Sciences USA 101: 1822818233.CrossRefGoogle ScholarPubMed
Pronina, N. A. & Borodin, V. V. (1993). CO2-stress and CO2 concentrating mechanism: Investigation by means of photosystem-deficient and carbonic anhydrase-deficient mutants of Chlamydomonas reinhardtii. Photosynthetica 28: 515522.Google Scholar
Pronina, N. A. & Semenenko, V. E. (1992). Pyrenoid role in CO2 concentration and fixation in microalga chloroplasts. Russian Journal of Plant Physiology 73: 723730.Google Scholar
Quigg, A., Finkel, Z. V., Irwin, A. J. et al. (2003). The evolutionary inheritance of elemental marine stoichiometry in marine phytoplankton. Nature 425: 291294.CrossRefGoogle ScholarPubMed
Quigg, A., Irwin, A. J. & Finkel, Z. V. (2011). Evolutionary inheritance of elemental stoichiometry in phytoplankton. Proceedings of the Royal Society of London B 278: 526534.Google ScholarPubMed
Ratti, S., Morse, D. & Giordano, M. (2007). CO2 concentrating mechanism of the potentially toxic dinoflagellate Protoceratium reticulatum (Dinophyceae, Gonyaulacales). Journal of Phycology 43: 693701.CrossRefGoogle Scholar
Ratti, S. & Giordano, M. (2008). Allocation of sulfur to sulfonium compounds in microalgae. In: Khan, N. A., Singh, S. & Umar, S. (eds.) Sulfur Assimilation and Abiotic Stress in Plants. Springer-Verlag, Berlin, pp. 317333.CrossRefGoogle Scholar
Ratti, S., Knoll, A. H. & Giordano, M. (2011). Did sulfate availability facilitate the evolutionary expansion of chlorophyll a+c phytoplankton in the oceans? Geobiology 9: 301312.CrossRefGoogle ScholarPubMed
Ratti, S., Knoll, A. H. & Giordano, M. (2013). Grazers and phytoplankton growth in the oceans: An experimental and evolutionary perspective. PLOS ONE 8: e77349.CrossRefGoogle ScholarPubMed
Raven, J. A. (1997a). Inorganic carbon acquisition by marine autotrophs. Advances in Botanical Research 27: 85209.CrossRefGoogle Scholar
Raven, J. A. (1997b). Putting the C in Phycology. European Journal of Phycology 32: 319333.CrossRefGoogle Scholar
Raven, J. A. (1997c). CO2 concentrating mechanisms: A role for thylakoid lumen acidification. Plant, Cell & Environment 20: 147154.CrossRefGoogle Scholar
Raven, J.A. (2009) Contribution of anoxygenic phototrophs and chemolithotrophs to carbon and oxygen fluxes in aquatic environments. Aquatic Microbial Ecology 56 : 177192.CrossRefGoogle Scholar
Raven, J. A. (2013). Half a century of pursuing the pervasive proton. Progress in Botany 74: 334.CrossRefGoogle Scholar
Raven, J. A. (2017). The possible roles of algae in restricting the increase in atmospheric CO2 and global temperature. European Journal of Phycology 52: 506522.CrossRefGoogle Scholar
Raven, J. A., Ball, L., Beardall, J. et al. (2005). Algae lacking CCMs. Canadian Journal of Botany 83: 879890.CrossRefGoogle Scholar
Raven, J. A. & Beardall, J. (2005). Respiration in aquatic photolithotrophs. In: del Giorgio, P. A. & Williams, P. J. le B. (eds.) Respiration in Aquatic Ecosystems. Oxford University Press, Oxford, UK. pp. 3646.CrossRefGoogle Scholar
Raven, J. A. & Beardall, J. (2003). CO2 acquisition mechanisms in algae: Carbon dioxide diffusion and carbon dioxide concentrating mechanisms. In: Larkum, A. W. D., Douglas, S. E. & Raven, J. A. (eds.) Photosynthesis in the Algae, Advances in Photosynthesis (Series Editor, Govindjee). Kluwer, Dordrecht/Boston/London. pp. 225244.CrossRefGoogle Scholar
Raven, J. A. & Beardall, J. (2016). The ins and outs of CO2. Journal of Experimental Botany 67: 113.CrossRefGoogle ScholarPubMed
Raven, J. A. & Beardall, J. (2017). Genotypic loss and phenotypic regulation of Complex I in mitochondria. Journal of Experimental Botany 68: 26832692.CrossRefGoogle Scholar
Raven, J. A., Beardall, J. & Giordano, M. (2014). Energy costs of carbon dioxide concentrating mechanisms. Photosynthesis Research 121: 111124.CrossRefGoogle ScholarPubMed
Raven, J. A., Beardall, J. & Griffiths, H. (1982). Inorganic C sources for Lemanea, Cladophora and Ranunculus in a fast-flowing stream: Measurements of gas exchange and of carbon isotope ratio and their ecological significance. Oecologia 53: 6878.CrossRefGoogle Scholar
Raven, J. A., Beardall, J. & Sánchez-Baracaldo, P. (2017). The possible evolution and future of CO2-concentrating mechanisms. Journal of Experimental Botany 68: 37013716.CrossRefGoogle ScholarPubMed
Raven, J. A., Cockell, C. S. & De La Rocha, C. L. (2008). The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philosophical Transactions of the Royal Society B 363: 26412650.CrossRefGoogle ScholarPubMed
Raven, J. A. & Colmer, T. D. (2016). Life at the boundary: Photosynthesis at the soil-liquid interface. A synthesis focusing on mosses. Journal of Experimental Botany 67: 16131623.CrossRefGoogle Scholar
Raven, J. A. & Giordano, M. (2017). Acquisition and metabolism of carbon in the Ochrophyta other than diatoms. Philosophical Transactions of the Royal Society B 372: 20160400.CrossRefGoogle ScholarPubMed
Raven, J. A., Giordano, M., Beardall, J. et al. (2011). Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynthesis Research 109: 281296.CrossRefGoogle ScholarPubMed
Raven, J. A., Giordano, M., Beardall, J. et al. (2012). Algal evolution in relation to atmospheric CO2: Carboxylases, carbon concentrating mechanisms and carbon oxidation cycles. Philosophical Transactions of the Royal Society B 367: 493507.CrossRefGoogle ScholarPubMed
Raven, J. A. & Hurd, C. J. (2012). Ecophysiology of photosynthesis in macroalgae. Photosynthesis Research 113: 105125CrossRefGoogle ScholarPubMed
Raven, J. A., Kübler, J. & Beardall, J. (2000). Put out the light, and then put out the light. Journal of the Marine Biological Association UK 80 (1): 125.CrossRefGoogle Scholar
Raven, J. A., Suggett, D. J. & Giordano, M. (2020). Inorganic carbon concentrating mechanisms in free-living and symbiotic dinoflagellates and chromerids. Journal of Phycology 56: 13771397.CrossRefGoogle ScholarPubMed
Reinfelder, J. R., Kraepiel, A. M. L. & Morel, F. M. M. (2000). Unicellular C4 photosynthesis in a marine diatom. Nature 407: 996999.CrossRefGoogle Scholar
Reinfelder, J. R., Milligan, A. J. & Morel, F. M. M. (2004). The role of C4 photosynthesis in carbon accumulation and fixation in a marine diatom. Plant Physiology 135: 21062111.CrossRefGoogle Scholar
Reiskind, J. B., Madsen, T. V., Van Ginke, L. C. et al. (1997). Evidence that inducible C4-like photosynthesis is a chloroplastic CO2-concentrating mechanism in Hydrilla, a submersed monocot. Plant, Cell & Environment 20: 211220.CrossRefGoogle Scholar
Reiskind, J. B., Seaman, P. T. & Bowes, G. (1988). Alternative methods of photosynthetic carbon assimilation in marine macroalgae. Plant Physiology 87: 686–92.CrossRefGoogle ScholarPubMed
Riding, R. (2006). Cyanobacterial calcification, carbon dioxide concentrating mechanisms, and Proterozoic–Cambrian changes in atmospheric composition. Geobiology 4: 299316.CrossRefGoogle Scholar
Roberts, K. Granum, E., Leegood, R. C. et al. (2007a). C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiology 145 : 230235.CrossRefGoogle Scholar
Roberts, K., Granum, E., Leegood, R. C. et al. (2007b). Carbon acquisition by diatoms. Photosynthesis Research 93: 7988.CrossRefGoogle ScholarPubMed
Rost, B., Riebesell, U., Burkhardt, S. et al. (2003). Carbon acquisition of bloom-forming marine phytoplankton. Limnology and Oceanography 48: 5567.CrossRefGoogle Scholar
Rotatore, C. & Colman, B. (1990). Uptake of inorganic carbon by isolated chloroplasts of the unicellular green alga Chlorella ellipsoidea. Plant Physiology 93: 1597–600.CrossRefGoogle ScholarPubMed
Rotatore, C. & Colman, B. (1991). The localization of active carbon transport at the plasma membrane in Chlorella ellipsoidea. Canadian Journal of Botany 69: 1025–31.CrossRefGoogle Scholar
Salvucci, M. E. & Bowes, G. (1983). Two photosynthetic mechanisms mediating the low photorespiratory state in submersed aquatic angiosperms. Plant Physiology 73: 488496.CrossRefGoogle Scholar
Schopf, J. W. (2011). The paleobiological record of photosynthesis. Photosynthesis Research 107: 87101.CrossRefGoogle Scholar
Scott, K. M., Henn-Sax, M., Harmer, T. L. et al. (2007). Kinetic isotope effect and biochemical characterization of form IA RubisCO from the marine cyanobacterium Prochlorococcus marinus MIT9313. Limnology and Oceanography 52(5): 21992204.CrossRefGoogle Scholar
Sharaf, A., Füssy, Z., Tomčala, A. et al. (2019). Isolation of plastids and mitochondria from Chromera velia. Planta 250: 17311741.CrossRefGoogle ScholarPubMed
Shen, Y., Canfield, D. E. & Knoll, A. H. (2002). Middle Proterozoic ocean chemistry: Evidence from the McArthur Basin, Northern Australia. American Journal of Science 302: 81109.CrossRefGoogle Scholar
Shibata, M., Katoh, H., Sonoda, M. et al. (2002). Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: Function and phylogenetic analysis. Journal of Biological Chemistry 277: 1865818664.CrossRefGoogle ScholarPubMed
Shiraiwa, Y., Danbara, A. & Yoke, K. (2004). Characterization of highly oxygen-sensitive photosynthesis in coccolithophorids. Japanese Journal of Phycology 52(Supplement): 8794.Google Scholar
Sinetova, M. A., Kupiyanova, E. V., Mankelova, A. G. et al. (2012). Identification and functional role of the carbonic anhydrase Cah3 in thylakoid membranes of pyrenoid of Chlamydomonas reinhardtii. Biochimica et Biophysica Acta 1817: 12481255.CrossRefGoogle ScholarPubMed
Smith, K. S. & Ferry, J. G. (2000). Prokaryotic carbonic anhydrases. FEMS Microbiology Reviews 24: 335366.CrossRefGoogle ScholarPubMed
Smith-Harding, T. J., Mitchell, J. G. & Beardall, J. (2017). The role of external carbonic anhydrase in photosynthesis during growth of the marine diatom Chaetoceros muelleri. Journal of Phycology 53: 11591170.CrossRefGoogle ScholarPubMed
Spalding, M. H., Critchley, C., Govindjee et al. (1984). Influence of carbon dioxide concentration during growth on fluorescence induction characteristics of the green alga Chlamydomonas reinhardtii. Photosynthesis Research 5: 169–76.CrossRefGoogle Scholar
Stefels, J. (2000). Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. Journal of Sea Research 43: 183197.CrossRefGoogle Scholar
Sunda, W. K. D. J., Kieber, D. J., Kiene, R. P. & Huntsman, S. (2002). An antioxidant function for DMSP and DMS in marine algae. Nature, 418: 317320.CrossRefGoogle ScholarPubMed
Suzuki, K., Onodera, H. (2005). Adaptation of a Chlamydomonas mutant with reduced rate of photorespiration to different concentrations of CO2. Canadian Journal of Botany 83: 834841.CrossRefGoogle Scholar
Tcherkez, G. G. B., Farquhar, G. D. & Andrews, T. J. (2006). Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proceedings of the National Academy of Science USA 103: 7246–725.CrossRefGoogle ScholarPubMed
Tchernov, D., Silverman, J., Luz, B. et al. (2003). Massive light-dependent cycling of inorganic carbon between oxygenic photosynthetic microorganisms and their surroundings. Photosynthesis Research 77: 95103.CrossRefGoogle ScholarPubMed
Tortell, P. (2000). Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnology and Oceanography 45: 744750.CrossRefGoogle Scholar
Trimborn, S., Lundholm, N., Thoms, S. et al. (2008). Inorganic carbon acquisition in potentially toxic and non-toxic diatoms: The effect of pH-induced changes in seawater carbonate chemistry. Physiologia Plantarum 133: 92105.CrossRefGoogle ScholarPubMed
Tsuji, Y., Mahardika, A. & Matsuda, Y. (2017a). Evolutionarily distinct strategies for the acquisition of inorganic carbon from seawater in marine diatoms. Journal of Experimental Botany 68: 39493958.CrossRefGoogle ScholarPubMed
Tsuji, Y., Nakajima, K. & Matsuda, Y. (2017b). Molecular aspects of the biophysical CO2-concentrating mechanism and its regulation in marine diatoms. Journal of Experimental Botany 68: 37633772.CrossRefGoogle ScholarPubMed
van Hunnik, E., Amoroso, G. & Sültemeyer, D. (2002). Uptake of CO2 and bicarbonate by intact cells and chloroplasts of Tetraedon minimum and Chlamydomonas noctigama. Planta 215: 763769.CrossRefGoogle ScholarPubMed
Vance, P. & Spalding, M. H. (2005). Growth, photosynthesis, and gene expression in Chlamydomonas over a range of CO2 concentrations and CO2/O2 ratios: CO2 regulates multiple acclimation states. Canadian Journal of Botany 83: 796809.CrossRefGoogle Scholar
Wang, Y., Stessman, D. J. & Spalding, M. H. (2015). The CO2 concentrating mechanism and photosynthetic carbon assimilation in limiting CO2: How Chlamydomonas works against the gradient. Plant Journal 82: 429448.CrossRefGoogle ScholarPubMed
Whitney, S., Shaw, D. & Yellowlees, D. (1995). Evidence that some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the α–proteobacteria. Proceedings of the Royal Society of London B 259: 271275.Google ScholarPubMed
Whitney, S. M. & Andrews, T. J. (1998). The CO2/O2 specificity of single-subunit ribulose-bisphosphate carboxylase from the dinoflagellate, Amphidinium carterae. Australian Journal of Plant Physiology 25: 131138.Google Scholar
Yamano, T., Sato, E., Iguchi, H. et al. (2015). Characterization of cooperative bicarbonate uptake into chloroplast stroma in the green alga. Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences USA 112: 73157320.CrossRefGoogle ScholarPubMed
Young, J. N., Heureux, A. M., Sharwood, R. E. et al. (2016). Large variation in the Rubisco kinetics of diatoms reveals diversity among their carbon-concentrating mechanisms. Journal of Experimental Botany 67: 34453456.CrossRefGoogle ScholarPubMed

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