Skip to main content

Acquisition of Inorganic Carbon by Microalgae and Cyanobacteria

  • Chapter
  • First Online:
Microbial Photosynthesis

Abstract

Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and the Calvin cycle are the dominant features of inorganic carbon assimilation in all cyanobacteria and microalgae. Rubisco carboxylase shows a relatively low affinity for CO2 and also has an oxygenase activity. These features can lead to inefficiencies in carbon assimilation, involving the process of photorespiration. However, cyanobacteria and algae possess mechanisms that minimise the effects of unfavourable Rubisco kinetics and photorespiration. These involve evolution of Rubiscos with kinetics that are more favourable to carboxylase activity and/or the presence of mechanisms that increase the concentration of CO2 at the active site of Rubisco (CO2 concentrating mechanisms, CCMs). CCMs are mostly based on active transport of HCO3. In one species of marine diatom, there appears to be a biochemical CCM where single cells show a C3–C4 intermediate form of C assimilation. In cyanobacteria HCO3 accumulation involves active transport of HCO3 at the plasmalemma and/or downhill CO2 entry with energised conversion of CO2 to HCO3 at the thylakoid membrane, with CO2 accumulated within carboxysomes that contain all of the cellular Rubisco as well as carbonic anhydrase. In eukaryotic microalgae active HCO3 transport occurs at either the plasmalemma or chloroplast envelope or both. In those algae that possess them, CO2 is ultimately concentrated within Rubisco-containing pyrenoids, though it is important to note that the presence of pyrenoids is not an absolute requirement for CCMs. Algae and cyanobacteria can assimilate inorganic carbon in the dark, a process reflecting the need of cells to replenish the supply of C4 intermediates of the TCA cycle as they are removed for biosynthesis. A few can also assimilate organic carbon sources, including in some cases by phagotrophy.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Amoroso, G., Sültemeyer, D. F., Thyssen, C., & Fock, H. P. (1998). Uptake of HCO3 and CO2 in cells and chloroplasts from the microalgae Chlamydomonas reinhardtii and Dunaliella tertiolecta. Plant Physiology, 116, 193–201.

    CAS  PubMed Central  Google Scholar 

  • Aono, R., Sato, T., Imanaka, T., & Atomi, H. (2015). A pentose bisphosphate pathway for nucleoside degradation in Archaea. Nature Chemical Biology, 11, 355–360.

    CAS  PubMed  Google Scholar 

  • 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, 3049–3059.

    CAS  PubMed  Google Scholar 

  • Badger, M. R., Andrews, T. J., Whitney, S. M., Ludwig, M., Yellowlees, D. C., Leggat, W., & Price, G. D. (1998). The diversity and coevolution of Rubiscos, plastids, pyrenoids and chloroplast-based CO2-concentrating mechanisms in algae. Canadian Journal of Botany, 76, 1052–1071.

    CAS  Google Scholar 

  • Bar-Even, A., Noor, E., Lewis, N. E., & Milo, R. (2010). Design and analysis of synthetic carbon fixation pathways. Proceedings of the National Academy of Sciences of the United States of America, 107, 8888–8894.

    Google Scholar 

  • Bar-Even, A., Noor, E., Savir, Y., Liebermeister, W., Davidi, D., Tawfik, D. S., & Milo, R. (2011). The moderately efficient enzyme: Evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry, 50, 4402–4404.

    CAS  PubMed  Google Scholar 

  • Bar-Even, A., Noor, E., & Milo, R. (2012). A survey of carbon fixation pathways through a quantitative lens. Journal of Experimental Botany, 63, 2325–2342.

    CAS  PubMed  Google Scholar 

  • Bathellier, C., Tcherkez, G., Lorimer, G. H., & Farquhar, G. D. (2018). Rubisco is not really so bad. Plant, Cell & Environment, 41, 705–716.

    CAS  Google Scholar 

  • Beardall, J., & Giordano, M. (2002). Ecological implications of microalgal and cyanobacterial CCMs and their regulation. Functional Plant Biology, 29, 335–347.

    CAS  PubMed  Google Scholar 

  • Beardall, J., & Raven, J. A. (2016). Carbon acquisition by microalgae. In M. Borowitzka, J. Beardall, & J. A. Raven (Eds.), The physiology of microalgae (pp. 89–100). Cham: Springer.

    Google Scholar 

  • Beardall, J., & Raven, J. A. (2019). Structural and biochemical features of carbon acquisition in algae. In A. W. D. Larkum, A. Grossman, & J. A. Raven (Eds.), Photosynthesis in the algae (Vol. 1, 2nd ed.). Dordrecht: Kluwer Academic Publishers. In press.

    Google Scholar 

  • Beardall, J., Mukerji, D., Glover, H. E., & Morris, I. (1976). The path of carbon in photosynthesis by marine phytoplankton. Journal of Phycology, 12, 409–417.

    CAS  Google Scholar 

  • Beardall, J., Quigg, A., & Raven, J. A. (2003). Oxygen consumption: Photorespiration and chlororespiration. In A. W. D. Larkum, S. E. Douglas, & J. A. Raven (Eds.), Photosynthesis in algae (pp. 157–181). Dordrecht: Kluwer.

    Google Scholar 

  • Behrenfeld, M. J., Randerson, J. T., McClain, C. R., Feldman, G. C., Los, S. O., Tucker, C. J., Falkowski, P. G., Field, C. B., Frouin, R., Esaias, W. E., Kolber, D. D., & Pollack, N. H. (2001). Biospheric primary production during an ENSO transition. Science, 291, 2594–2597.

    CAS  PubMed  Google Scholar 

  • Bhatti, S., & Colman, B. (2008). Inorganic carbon acquisition in some synurophyte algae. Physiologia Plantarum, 133, 33–40.

    CAS  PubMed  Google Scholar 

  • Blanc, G., Agarkova, I., Grimwood, J., Kuo, A., Brueggeman, A., Dunigan, D. D., Gurnon, J., Ladunga, I., Lindquist, E., Lucas, S., Pangilinan, J., Pröschold, T., Salamov, A., Schmutz, J., Weeks, D., Yamada, T., Lomsadze, A., Borodovsky, M., Claverie, J. M., Grigoriev, I. V., & Van Etten, J. L. (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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boggetto, N., Gontero, B., & Maberly, S. C. (2007). Regulation of phosphoribulokinase and glyceraldehyde 3-phosphate dehydrogenase in a freshwater diatom, Asterionella formosa. Journal of Phycology, 43, 1227–1235.

    CAS  Google Scholar 

  • Boller, A. J., Thomas, P. J., Cavenaugh, C. M., & Scott, K. M. (2011). Low stable isotope fractionation by coccolithophore RuBISCO. Geochimica et Cosmochimica Acta, 75, 7200–7207.

    CAS  Google Scholar 

  • Bonar, P. T., & Casey, J. R. (2008). Plasma membrane Cl/HCO3 exchangers: Structure, mechanism and physiology. Channels, 2, 337–345.

    PubMed  Google Scholar 

  • Burkhardt, S., Amoroso, G., Riebesell, U., & Sültemeyer, D. (2001). CO2 and HCO3 uptake in marine diatoms acclimated to different CO2 concentrations. Limnology and Oceanography, 46, 1378–1391.

    CAS  Google Scholar 

  • Chi, S., Wu, S., Yu, J., Wang, X., Tang, X., & Liu, T. (2014). Phylogeny of C4-photosynthesis enzymes based on algal transcriptomic and genomic data supports an archaeal/proteobacterial origin and multiple duplication for most C4-related genes. PLoS One, 9, e110154.

    PubMed  PubMed Central  Google Scholar 

  • Colman, B., & Rotatore, C. (1995). Photosynthetic inorganic carbon uptake and accumulation in two marine diatoms. Plant, Cell & Environment, 18, 919–924.

    CAS  Google Scholar 

  • Di Mario, R. J., Machingura, M. C., Waldrop, G. L., & Moroney, J. V. (2017). The many types of carbonic anhydrases in photosynthetic organisms. Plant Science, 268, 11–17.

    Google Scholar 

  • Dodge, J. D. (1973). The fine structure of algal cells. London: Academic Press.

    Google Scholar 

  • Eisenhut, M., Ruth, W., Haimovitch, M., Bauwe, M., Kaplan, A., & Hagemann, M. (2008). The photorespiratory glycolate metabolism is essential for cyanobacteria and may have been conveyed endosymbiotically to plants. Proceedings of the National Academy of Sciences of the United States of America, 105, 17199–17204.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Engel, B. D., Schaffer, M., Kuhn Cuellar, L., Villa, E., Plitzko, J. M., & Baumeister, W. (2015). Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography. eLife, 4, e04889.

    PubMed  PubMed Central  Google Scholar 

  • Falkowski, P. G., & Raven, J. A. (2007). Aquatic photosynthesis (2nd ed.). Princeton: Princeton University Press.

    Google Scholar 

  • Flynn, K. J., Stoecker, D. K., Mitra, A., Raven, J. A., Glibert, P. M., Hansen, P. J., Granéli, E., & Burkholder, J. M. (2013). A case of mistaken identification: The importance of mixotrophs and the clarification of plankton functional-classification. Journal of Plankton Research, 35, 3–11. https://doi.org/10.1093/plankt/fbs062.

    Article  Google Scholar 

  • Frolov, E. N., Kublanov, I. V., Toshchakov, S. V., Lunev, E. A., Pimenov, N. V., Bonch-Osmolovskaya, E. A., Lebedinsky, A. V., & Chernyh, N. A. (2019). Form III RubisCO-mediated transaldolase variant of the Calvin cycle in a chemolithoautotrophic bacterium. Proceedings of the National Academy of Sciences of the United States of America, 116(37), 18638–18646. https://doi.org/10.1073/pnas.1904225116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuchs, G. (2011). Alternative pathways of carbon dioxide fixation: Insights into the early evolution of life? Annual Review of Microbiology, 65, 631–658.

    CAS  PubMed  Google Scholar 

  • 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 of the United States of America, 114, 4537–4542.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Giordano, M., Beardall, J., & Raven, J. A. (2005). CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology, 6, 99–131.

    Google Scholar 

  • Griffiths, H., Meyer, M. T., & Rickaby, R. E. M. (2017). Overcoming adversity through diversity: Aquatic carbon concentrating mechanisms. Journal of Experimental Botany, 68, 3689–3695.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haimovich-Dayan, M., Garfinkel, N., Ewe, D., Marcus, Y., Gruber, A., Wagner, H., Kroth, P. G., & Kaplan, A. (2013). The role of C4 metabolism in the marine diatom Phaeodactylum tricornutum. The New Phytologist, 197, 177–185.

    CAS  PubMed  Google Scholar 

  • Hopkinson, B. M., Dupont, C. L., Allen, A. E., & Morel, M. M. (2011). Efficiency of the CO2-concentrating mechanism in diatoms. Proceedings of the National Academy of Sciences of the United States of America, 108, 3830–3837.

    CAS  PubMed  PubMed Central  Google 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, 1142–1152.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huertas, I. E., Colman, B., & Espie, G. S. (2002). Inorganic carbon acquisition and its energization in eustigmatophyte algae. Functional Plant Biology, 29, 271–277.

    CAS  PubMed  Google Scholar 

  • Jensen, E., Clement, R., Maberly, S., & Gontero, B. (2017). Regulation of the Calvin–Benson–Bassham cycle in the enigmatic diatoms: Biochemical and evolutionary variations on an original theme. Philosophical Transactions of the Royal Society of London B, 372, 20160401.

    Google Scholar 

  • Jensen, E., Clement, R., Kosta, A., Maberly, S. C., & Gontero, B. (2019). A new widespread subclass of carbonic anhydrase in marine phytoplankton. The ISME Journal, 13, 2094–2106.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 988–990.

    CAS  Google Scholar 

  • Johnston, A. M., & Raven, J. A. (1996). Inorganic carbon accumulation by the marine diatom Phaeodactylum tricornutum. European Journal of Phycology, 31, 285–290.

    Google Scholar 

  • Kaldenhoff, R., Kai, L., & Uehlein, N. (2014). Aquaporins and membrane diffusion of CO2 in living organisms. Biochimica et Biophysica Acta, 1840, 1592–1595.

    CAS  PubMed  Google Scholar 

  • Kevekordes, K., Holland, D., Jenkins, S., Koss, R., Roberts, S., Raven, J. A., Scrimgeour, C. M., Shelly, K., Stojkovic, S., & Beardall, J. (2006). Inorganic carbon acquisition by eight species of Caulerpa. Phycologia, 45, 442–449.

    Google Scholar 

  • Kikutani, S., Nakajima, K., Nagasato, C., Tsuji, Y., Miyatake, A., & Matsuda, Y. (2016). Thylakoid luminal θ-carbonic anhydrase critical for growth and photosynthesis in the marine diatom Phaeodactylum tricornutum. Proceedings of the National Academy of Sciences of the United States of America, 113, 9828–9833.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Korb, R. E., Saville, P. J., Johnston, A. M., & Raven, J. A. (1997). Sources of inorganic carbon for photosynthesis by three species of marine diatoms. Journal of Phycology, 33, 433–440.

    CAS  Google Scholar 

  • Kübler, J. E., & Raven, J. A. (1994). Consequences of light limitation for carbon acquisition in three rhodophytes. Marine Ecology Progress Series, 110, 203–209.

    Google 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, 369–375.

    Google 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, 1427–1436.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 1247–1255.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maberly, S. C., Ball, L. A., Raven, J. A., & Sültemeyer, D. (2009). Inorganic carbon acquisition by chrysophytes. Journal of Phycology, 45, 1057–1061.

    Google Scholar 

  • Maberly, S. C., Courcelle, C., Grobden, R., & Gontero, B. (2010). Phylogenetically-based variation in the regulation of the Calvin cycle enzymes, phosphoribulokinase and glyceraldehyde-3-phosphate dehydrogenase, in algae. Journal of Experimental Botany, 61, 735–745.

    CAS  PubMed  Google Scholar 

  • Machingura, M. C., Bajsa-Hirschel, J., Laborde, S. M., Schwartzenburg, J. B., Mukherjee, B., Mukherjee, A., Pollock, S. V., Förster, B., Price, G. D., & Moroney, J. V. (2017). Identification and characterization of a solute carrier, CIA8, involved in inorganic carbon acclimation in Chlamydomonas reinhardtii. Journal of Experimental Botany, 68, 3879–3890.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mackinder, L. C. M. (2018). The Chlamydomonas CO2-concentrating mechanism and its potential for engineering photosynthesis in plants. The New Phytologist, 217, 54–61.

    CAS  PubMed  Google Scholar 

  • Mackinder, L., Chen, C., Leib, R., Patena, W., Blum, S. R., Rodman, M., Ramundo, S., Adams, C. M., & Jonikas, M. C. (2017). A spatial interactome reveals the protein organization of the algal CO2 concentrating mechanism. Cell, 171, 133–147.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuda, Y., Hopkinson, B. M., Nakajima, K., Dupont, C. L., & Tsuji, Y. (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.

    Google Scholar 

  • McKay, R. M. L., & Gibbs, S. P. (1991). Composition and function of pyrenoids: Cytochemical and immunocytochemical approaches. Canadian Journal of Botany, 69, 1040–1052.

    CAS  Google Scholar 

  • Meyer, M., & Griffiths, H. (2013). Origins and diversity of eukaryotic CO2-concentrating mechanisms: Lessons for the future. Journal of Experimental Botany, 64, 769–786.

    CAS  PubMed  Google Scholar 

  • Meyer, M. T., Whittaker, C., & Griffiths, H. (2017). The algal pyrenoid: Key unanswered questions. Journal of Experimental Botany, 68, 3739–3749.

    CAS  PubMed  Google Scholar 

  • Michels, A. K., Wedel, N., & Kroth, P. G. (2005). Diatom plastids possess a phosphoribulokinase with an altered regulation and no oxidative pentose phosphate pathway. Plant Physiology, 137, 911–920.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchell, C., & Beardall, J. (1996). Inorganic carbon uptake by an Antarctic sea-ice diatom, Nitzschia frigida. Polar Biology, 21, 310–315.

    Google Scholar 

  • Morel, F. M. M., Cox, E. H., Kraepiel, A. M. L., Lane, T. W., Milligan, A. J., Schaperdoth, I., Reinfelder, J. R., & Tortell, P. D. (2002). Acquisition of inorganic carbon by the marine diatom Thalassiosira weissflogii. Functional Plant Biology, 29, 301–308.

    CAS  PubMed  Google Scholar 

  • Morita, E., Abe, T., Tsuzuki, M., Fujiwara, S., Sato, N., Hirata, A., Sonoike, K., & Nozaki, H. (1998). Presence of the CO2-concentrating mechanism in some species of the pyrenoid-less free-living algal genus Chloromonas (Volvocales, Chlorophyta). Planta, 204, 269–276.

    CAS  PubMed  Google Scholar 

  • Morita, E., Abe, T., Tsuzuki, M., Fujiwara, S., Sato, N., Hirata, A., Sonoike, K., & Nozaki, H. (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, 365–372.

    Google Scholar 

  • Morris, I., Yentsch, C. M., & Yentsch, C. S. (1971). Relationship between light carbon dioxide fixation and dark carbon dioxide fixation by marine algae. Limnology and Oceanography, 16, 854–858.

    Google Scholar 

  • Morris, I., Beardall, J., & Mukerji, D. (1978). The mechanisms of carbon fixation in phytoplankton. Mitt Internat Verein Limnol, 21, 174–183.

    CAS  Google Scholar 

  • Mukherjee, A., Lau, C. S., Walker, C. E., Rai, A. K., Prejean, C. I., Yates, G., Emrich-Mills, T., Lemoine, S. G., Vinyard, D. J., Mackinder, L. C. M., & Moroney, J. V. (2019). Thylakoid localized bestrophin-like proteins are essential for the CO2 concentrating mechanism of Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences of the United States of America 116, 16915–16920.

    Google Scholar 

  • Munoz, J., & Merrett, M. J. (1989). Inorganic carbon transport in some marine eukaryotic microalgae. Planta, 178, 450–455.

    CAS  PubMed  Google Scholar 

  • 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 of the United States of America, 110, 1767–1772.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ogawa, T., & Ogren, W. L. (1985). Action spectra for accumulation of inorganic carbon in the cyanobacterium, Anabaena variabilis. Photochemistry and Photobiology, 41, 583–587.

    CAS  Google Scholar 

  • Ogawa, T., Miyano, A., & Inoue, Y. (1985). Photosystem-I-driven inorganic carbon transport in the cyanobacterium, Anacystis nidulans. Biochimica et Biophysica Acta, 808, 74–75.

    Google Scholar 

  • Ohnishi, N., Mukherjee, B., Tsujikawa, T., Yanase, M., Nakano, H., Moroney, J. V., & Fukuzawa, H. (2010). Expression of a low CO2-inducible protein, LCI1, increases inorganic carbon uptake in the green alga Chlamydomonas reinhardtii. Plant Cell, 22, 3105–3311.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Omata, T., Price, G. D., Badger, M. R., Okamura, M., Gohta, S., & Ogawa, T. (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 of the United States of America, 96, 13571–13576.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palmqvist, K., Sundblad, L.-G., Wingsle, G., & Samuelsson, G. (1990). Acclimation of photosynthetic light reactions during induction of inorganic carbon accumulation in the green alga Chlamydomonas reinhardtii. Plant Physiology, 94, 357–366.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Patel, B. N., & Merrett, M. J. (1986). Regulation of carbonic anhydrase activity, inorganic carbon uptake and photosynthetic biomass yield in Chlamydomonas reinhardtii. Planta, 169, 81–86.

    CAS  Google Scholar 

  • Price, G. D., & Badger, M. R. (1989). Expression of human carbonic anhydrase in the cyanobacterium Synechocystis PCC7942 creates a high CO2-requiring phenotype. Plant Physiology, 91, 505–513.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Price, G. D., Maeda, S., Omata, T., & Badger, M. (2002). Modes of active inorganic carbon uptake in the cyanobacterium Synechococcus sp. PCC7942. Functional Plant Biology, 29, 131–149.

    CAS  PubMed  Google Scholar 

  • Price, G. D., Woodger, F. J., Badger, M. R., Howitt, S. M., & Tucker, L. (2004). Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proceedings of the National Academy of Sciences of USA, 101, 18228–18233.

    CAS  Google Scholar 

  • Price, G. D., Badger, M. R., Woodger, F. J., & Long, B. J. (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, 1441–1461.

    CAS  PubMed  Google Scholar 

  • Raven, J. A. (1997a). Inorganic carbon acquisition by marine autotrophs. Advances in Botanical Research, 27, 85–209.

    CAS  Google Scholar 

  • Raven, J. A. (1997b). Putting the C in phycology. European Journal of Phycology, 32, 319–333.

    Google Scholar 

  • Raven, J. A. (1997c). CO2 concentrating mechanisms: A role for thylakoid lumen acidification. Plant, Cell & Environment, 20, 147–154.

    CAS  Google Scholar 

  • Raven, J. A. (2009). Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquatic Microbial Ecology, 56, 177–192.

    Google Scholar 

  • Raven, J. A., & Beardall, J. (2003). CO2 acquisition mechanisms in algae: Carbon dioxide diffusion and carbon dioxide concentrating mechanisms. In A. W. D. Larkum, S. E. Douglas, & J. A. Raven (Eds.), Photosynthesis in the algae (pp. 225–244). Dordrecht: Kluwer Academic Publishers.

    Google Scholar 

  • Raven, J. A., & Beardall, J. (2005). Respiration in aquatic photolithotrophs. In P. A. del Giorgio & P. J. L. B. Williams (Eds.), Respiration in aquatic ecosystems (pp. 36–46). Oxford: Oxford University Press.

    Google Scholar 

  • Raven, J. A., & Beardall, J. (2014). CO2 concentrating mechanisms and environmental change. Aquatic Botany, 118, 24–37.

    CAS  Google Scholar 

  • Raven, J. A., & Beardall, J. (2016a). Dark respiration and organic carbon loss. In M. Borowitzka, J. Beardall, & J. A. Raven (Eds.), The physiology of microalgae (pp. 129–142). Cham: Springer.

    Google Scholar 

  • Raven, J. A., & Beardall, J. (2016b). The ins and outs of CO2. Journal of Experimental Botany, 67, 1–13.

    CAS  PubMed  Google Scholar 

  • 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, 1613–1623.

    CAS  PubMed  Google Scholar 

  • Raven, J. A., & Giordano, M. (2017). Acquisition and metabolism of carbon in the Ochrophyta other than diatoms. Philosophical Transactions of the Royal Society of London B, 372, 20160400.

    Google Scholar 

  • 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, 68–78.

    PubMed  Google Scholar 

  • Raven, J. A., Ball, L., Beardall, J., Giordano, M., & Maberly, S. C. (2005). Algae lacking CCMs. Canadian Journal of Botany, 83, 879–890.

    CAS  Google Scholar 

  • 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 of London B, 363, 2641–2650.

    CAS  Google Scholar 

  • Raven, J. A., Beardall, J., Flynn, K. J., & Maberly, S. C. (2009). Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: Relation to Darwin’s insectivorous plants. Journal of Experimental Botany, 60, 3975–3987. https://doi.org/10.1093/jxb/erp282.

    Article  CAS  PubMed  Google Scholar 

  • Raven, J. A., Giordano, M., Beardall, J., & Maberly, S. (2011). Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynthesis Research, 109, 281–296.

    CAS  PubMed  Google Scholar 

  • Raven, J. A., Giordano, M., Beardall, J., & Maberly, S. C. (2012). Algal evolution in relation to atmospheric CO2: Carboxylases, carbon concentrating mechanisms and carbon oxidation cycles. Philosophical Transactions of the Royal Society B, 367, 493–507.

    CAS  Google Scholar 

  • Raven, J. A., Beardall, J., & Giordano, M. (2014). Energy costs of carbon dioxide concentrating mechanisms. Photosynthesis Research, 121, 111–124.

    CAS  PubMed  Google Scholar 

  • Raven, J. A., Beardall, J., & Quigg, A. (2019). Light-driven oxygen consumption in the water-water cycles and photorespiration, and light stimulated mitochondrial respiration. In A. W. D. Larkum, A. R. Grossman, & J. A. Raven (Eds.), Photosynthesis in Algae (2nd ed.). Berlin: Springer. In press.

    Google Scholar 

  • Reinfelder, J. R. (2011). Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annual Review of Marine Science, 3, 291–315.

    PubMed  Google Scholar 

  • Reinfelder, J. R., Kraepiel, A. M. L., & Morel, F. M. M. (2000). Unicellular C4 photosynthesis in a marine diatom. Nature, 407, 996–999.

    CAS  PubMed  Google 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, 2106–2111.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reiskind, J. B., Seaman, P. T., & Bowes, G. (1988). Alternative methods of photosynthetic carbon assimilation in marine macroalgae. Plant Physiology, 87, 686–692.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts, K., Granum, E., Leegood, R. C., & Raven, J. A. (2007a). C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiology, 145, 230–235.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts, K., Granum, E., Leegood, R. C., & Raven, J. A. (2007b). Carbon acquisition by diatoms. Photosynthesis Research, 93, 79–88.

    CAS  PubMed  Google Scholar 

  • Rost, B., Riebesell, U., Burkhardt, S., & Sültemeyer, D. (2003). Carbon acquisition of bloom-forming marine phytoplankton. Limnology and Oceanography, 48, 55–67.

    Google Scholar 

  • Rost, B., Kranz, S. A., Richter, K.-U., & Tortell, P. D. (2007). Isotope disequilibrium and mass spectrometric studies of inorganic carbon acquisition by phytoplankton. Limnology and Oceanography: Methods, 5, 328–337.

    CAS  Google Scholar 

  • Rotatore, C., & Colman, B. (1990). Uptake of inorganic carbon by isolated chloroplasts of the unicellular green alga Chlorella ellipsoidea. Plant Physiology, 93, 1597–1600.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rotatore, C., & Colman, B. (1991). The localization of active carbon transport at the plasma membrane in Chlorella ellipsoidea. Canadian Journal of Botany, 69, 1025–1031.

    CAS  Google Scholar 

  • Scott, K. M., Henn-Sax, M., Harmer, T. L., Longo, D. L., Frome, C. H., & Cavenaugh, C. M. (2007). Kinetic isotope effect and biochemical characterisation of form IA Rubisco from the marine cyanobacterium Prochlorococcus marinus MIT9313. Limnology and Oceanography, 55, 2199–2204.

    Google Scholar 

  • Shibata, M., Katoh, H., Sonoda, M., Ohkawa, H., Shimoyama, M., Fukuzawa, H., Kaplan, A., & Ogawa, T. (2002). Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: Function and phylogenetic analysis. The Journal of Biological Chemistry, 277, 18658–18664.

    CAS  PubMed  Google Scholar 

  • Shiraiwa, Y., Danbara, A., & Yoke, K. (2004). Characterization of highly oxygen-sensitive photosynthesis in coccolithophorids. Japanese Journal of Phycology, 52(Supplement), 87–94.

    Google Scholar 

  • Smith, K. S., & Ferry, J. G. (2000). Prokaryotic carbonic anhydrases. FEMS Microbiology Reviews, 24, 335–366.

    CAS  PubMed  Google Scholar 

  • 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, 1159–1170.

    Google Scholar 

  • Spalding, M. H., Critchley, C., Govindjee, & Ogren, W. L. (1984). Influence of carbon dioxide concentration during growth on fluorescence induction characteristics of the green alga Chlamydomonas reinhardtii. Photosynthesis Research, 5, 169–176.

    CAS  PubMed  Google Scholar 

  • Stojkovic, S., Beardall, J., & Matear, R. (2013). CO2 concentrating mechanisms in three southern hemisphere strains of Emiliania huxleyi. Journal of Phycology, 49, 670–679.

    CAS  PubMed  Google Scholar 

  • Tcherkez, G. G. B., Farqhar, 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 Sciences of the United States of America, 103, 7246–7725.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tchernov, D., Silverman, J., Luz, B., Reinhold, L., & Kaplan, A. (2003). Massive light-dependent cycling of inorganic carbon between oxygenic photosynthetic microorganisms and their surroundings. Photosynthesis Research, 77, 95–103.

    CAS  PubMed  Google Scholar 

  • Tortell, P. (2000). Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnology and Oceanography, 45, 744–750.

    CAS  Google Scholar 

  • Trimborn, S., Lundholm, N., Thoms, S., Richter, K. U., Krock, B., Hansen, P. J., & Rost, B. (2008). Inorganic carbon acquisition in potentially toxic and non-toxic diatoms: The effect of pH-induced changes in seawater carbonate chemistry. Physiologia Plantarum, 133, 92–105.

    CAS  PubMed  Google Scholar 

  • Tsuji, Y., Suzuki, I., & Shiraiwa, Y. (2009). Photosynthetic carbon assimilation in the coccolithophorid Emiliania huxleyi (Haptophyta): Evidence for the predominant operation of the C3 cycle and the contribution of β-carboxylases to the active anaplerotic reaction. Plant & Cell Physiology, 50, 318–329.

    CAS  Google Scholar 

  • Tsuji, Y., Suzuki, I., & Shiraiwa, Y. (2012). Enzymological evidence for the function of a plastid-located pyruvate carboxylase in the haptophyte alga Emiliania huxleyi: A novel pathway for the production of C4 compounds. Plant & Cell Physiology, 53, 1043–1052.

    CAS  Google Scholar 

  • 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, 3949–3958.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 3763–3772.

    CAS  PubMed  Google Scholar 

  • 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, 763–769.

    PubMed  Google Scholar 

  • Villarejo, A., Martinez, F., del Pino Plumed, M., & Ramazanov, Z. (1996). The induction of the CO2 concentrating mechanism in a starch-less mutant of Chlamydomonas reinhardtii. Physiologia Plantarum, 98, 798–802.

    CAS  Google 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, 429–448.

    PubMed  Google Scholar 

  • 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, 131–138.

    CAS  Google Scholar 

  • Whitney, S., Shaw, D., & Yellowlees, D. (1995). Evidence that some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the alpha-proteobacteria. Proceedings of the Royal Society of London B, 259, 271–275.

    CAS  Google Scholar 

  • Yamano, T., Sato, E., Iguchi, H., Fukuda, Y., & Fukuzawa, H. (2015). Characterization of cooperative bicarbonate uptake into chloroplast stroma in the green alga Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences of the United States of America, 112, 7315–7320.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Young, J. N., Heureux, A. M., Sharwood, R. E., Rickaby, R. E., Morel, F. M., & Whitney, S. M. (2016). Large variation in the Rubisco kinetics of diatoms reveals diversity among their carbon-concentrating mechanisms. Journal of Experimental Botany, 67, 3445–3456.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John Beardall .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Beardall, J., Raven, J.A. (2020). Acquisition of Inorganic Carbon by Microalgae and Cyanobacteria. In: Wang, Q. (eds) Microbial Photosynthesis. Springer, Singapore. https://doi.org/10.1007/978-981-15-3110-1_8

Download citation

Publish with us

Policies and ethics