Skip to main content
SpringerLink
Log in

Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Minimum energy (as photon) costs are predicted for core reactions of photosynthesis, for photorespiratory metabolism in algae lacking CO2 concentrating mechanisms (CCMs) and for various types of CCMs; in algae, with CCMs; allowance was made for leakage of CO2 from the internal pool. These predicted values are just compatible with the minimum measured photon costs of photosynthesis in microalgae and macroalgae lacking or expressing CCMs. More energy-expensive photorespiration, for example for organisms using Rubiscos with lower CO2–O2 selectivity coefficients, would be less readily accommodated within the lowest measured photon costs of photosynthesis by algae lacking CCMs. The same applies to the cases of CCMs with higher energy costs of active transport of protons or inorganic carbon species, or greater allowance for significant leakage from the accumulated intracellular pool of CO2. High energetic efficiency can involve a higher concentration of catalyst to achieve a given rate of reaction, adding to the resource costs of growth. There are no obvious mechanistic interpretations of the occurrence of CCMs algae adapted to low light and low temperatures using the rationales adopted for the occurrence of C4 photosynthesis in terrestrial flowering plants. There is an exception for cyanobacteria with low-selectivity Form IA or IB Rubiscos, and those dinoflagellates with low-selectivity Form II Rubiscos, for which very few natural environments have high enough CO2:O2 ratios to allow photosynthesis in the absence of CCMs.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Atkinson MR, Smith SV (1983) C:N:P ratios of benthic marine plants. Limnol Oceanogr 28:569–571

    Google Scholar 

  • Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622

    CAS  PubMed  Google Scholar 

  • Badger MR, Bassett M, Comins HN (1985) A model for HCO3 − accumulation and photosynthesis in the cyanobacterium Synechococcus sp. Plant Physiol 77:465–471

    Google Scholar 

  • Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W, Price GD (1998) The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can J Bot 76:1052–1071

    CAS  Google Scholar 

  • Beardall J (1991) Effects of photon flux density on the CO2-concentrating mechanism of the cyanobacterium Anabaena variabilis. J Plankton Res 13:133–141

    Google Scholar 

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

    CAS  Google Scholar 

  • Beer S, Bjork M, Hellblom F, Axelsson L (2002) Inorganic carbon utilization by marine angiosperms (seagrasses). Funct Plant Biol 29:349–354

    CAS  Google Scholar 

  • Blank CE, Sanchez-Baracaldo P (2010) Timing of morphological and ecological innovations in the cyanobacteria—a key to understanding the rise of atmospheric oxygen. Geobiology 8:1–23

    CAS  PubMed  Google Scholar 

  • Bowes G, Rao SK, Estravillo GM, Reiskind JB (2002) C4 mechanisms in aquatic angiosperms: comparisons with terrestrial C4 systems. Funct Plant Biol 29:379–382

    CAS  Google Scholar 

  • Brechignac F, Lucas WJ (1987) Photorespiration and internal CO2 accumulation in Chara coralline as inferred from the influence of DIC and O2 on photosynthesis. Plant Physiol 83:163–169

    CAS  PubMed Central  PubMed  Google Scholar 

  • Briskin DP, Reynolds-Nielman I (1991) Determination of the H+-ATP stoichiometry for the plasma membrane H+-ATPase from red beet (Beta vulgaris) storage tissue. Plant Physiol 93:242–250

    Google Scholar 

  • Cassar N, Laws EA (2007) Potential contribution of β-carboxylases to photosynthetic carbon isotope fractionation in a marine diatom. Phycologia 44:393–402. doi:10.2216/06-50.1

    Google Scholar 

  • Collins E, Wong CY, Wilk KE, Curmi PMG, Brumer P, Scholes GD (2010) Coherently wired light harvesting in photosynthetic marine algae at ambient temperature. Nature 463:644–647

    Google Scholar 

  • Eisenhut M, Ruth W, Haimovitch M, Bauwe H, Kaplan A, Hagemannn H (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been transferred endosymbiotically to plants. Proc Natl Acad Sci USA 1085:17190–17204

    Google Scholar 

  • Fabris M, Matthijs M, Rombouts S, Vyverman W, Goosers A, Baart GJE (2012) The metabolic blueprint of Phaeodactylum tricornutum reveals a eukaryotic Entner-Doudoroff pathway glycolytic pathway. Plant J 20:1004–1014

    Google Scholar 

  • Falkowski PG, Raven JA (2007) Aquatic Photosynthesis, 2nd  edn. Princeton University Press, Princetion, 484pp

  • Ferrier JM (1980) Apparent bicarbonate use and possible plasmalemma proton efflux in Chara corallna. Plant Physiol 66:1198–1199

    CAS  PubMed Central  PubMed  Google Scholar 

  • Flamholz A, Noor E, Bar-even A, Liebermeister W, Milo R (2013) Glycolytic strategy as a trade off between energy yield and protein cost. Proc Natl Acad Sci USA 110:10039–10044. doi:10.1073/pnas.1215283110

    CAS  PubMed Central  PubMed  Google Scholar 

  • Flynn KJ, Blackford JC, Baird ME, Raven JA, Clark DR, Beardall J, Brownlee C, Fabian H, Wheeler GL (2012) Changes in pH at the exterior surface of plankton with ocean acidification. Nat Clim Change 2:510–513

    CAS  Google Scholar 

  • Geider RJ, Osborne BA, Raven JA (1985) Light dependence of growth and photosynthesis in Phaeodactylum tricornutum (Bacillariophyceae). J Phycol 21:609–619

    Google Scholar 

  • Geider RJ, Osborne BA, Raven JA (1986) Growth, photosynthesis and maintenance metabolic costs in the diatom Phaeodactylum tricornutum at very low light levels. J Phycol 22:39–48

    Google Scholar 

  • Gillies CL, Stark JS, Johnstone JI, Smith SDA (2012) Carbon flow and trophic structure of an Antarctic coastal benthic community as determined by δ13C and δ15N. Estuar Coast Shelf Sci 97:44–57

    CAS  Google Scholar 

  • Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation and evolution. Annu Rev Plant Biol 56:99–131

    CAS  PubMed  Google Scholar 

  • Granum E, Raven JA, Leegood RC (2005) How do marine diatoms fix ten billion tonnes of inorganic carbon per year? Can J Bot 83:898–908

    CAS  Google Scholar 

  • Granum E, Roberts K, Raven JA, Leegood RC (2009) Primary carbon and nitrogen metabolic gene expression in the diatom Thalassiosira pseudonana (Bacillariophyceae): diel periodicity and effects of inorganic carbon and nitrogen. J Phycol 45:1083–1092. doi:10.1111/j/1529-8817.2009.22728.x

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Haslam RP, Keys AJ, Androlajc PJ, Madgwick PJ, Amdersson I, Grimsrud A, Eilertsen HC, Parry MAJ (2005) Specificity of diatom rubisco. In: Awasa A, Nouchi I, De Kok LJ (eds) Plant responses to air pollution and global change. Springer, Tokyo, pp 157–164

    Google Scholar 

  • Hellblom E, Beer S, Bjork M, Axelsson L (2001) A buffer sensitive inorganic carbon utilization system in Zostera marina. Aquatic Bot 69:55–62

    CAS  Google Scholar 

  • Hepburn CD, Pritchard DW, Cornwall CE, McLeod RJ, Beardall J, Raven JA, Hurd CL (2011) Diversity of carbon use strategies in a kelp forest community: a window to a high CO2 ocean? Global Change Biol 17:2488–2497

    Google Scholar 

  • Hildner R, Brinks D, Nieder JR, Cogdell RJ, van Hulst HF (2011) Quantum coherent energy transfer under varying pathways in single light-harvesting complexes. Science 340:1448–1451

    Google Scholar 

  • Hogewoning SW, Wientjes E, Douwstra P, Trouwborst G, von Ieperen W, Grace R, Harbinson J (2012) Photosynthetic quantum yield dynamics: from photosynthesis to leaves. Plant Cell 24:1921–1936. doi:10.1105/tpc.112.097972

    CAS  PubMed Central  PubMed  Google Scholar 

  • Holaday AS, Bowes G (1980) C4 acid metabolism and dark CO2 fixation in a submersed aquatic macrophyte (Hydrilla verticillata). Plant Physiol 65:331–335

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hopkinson BM, Dupont CL, Allen AE, Morel FMM (2011) Efficiency of the CO2-concentraing mechanism of diatoms. Proc Natl Acad Dvi USA 108:3830–3837

    CAS  Google Scholar 

  • Hossein-Nejad H, Curutchet C, Schols KA, Scholes GD (2011) Delocalization enhanced long-range energy transfer between PE545 antenna proteins. J Physical Chem B 115:5243–5253

    CAS  Google Scholar 

  • Johnsen G, Sakshaug E (2007) Biooptical characteristics of PSII and PSI in 33 species (13 pigment groups) of marine phytoplankton and the relevance for pulse-amplitude-modulated and fast-repetition-rate fluorometry. J Phycol 43:1236–1251. doi:10.1111/j.1529-8817.2007.0042x

    CAS  Google Scholar 

  • Johnston AM, Maberly SC, Raven JA (1992) The acquisition of inorganic carbon by four red macroalgae from different habitats. Oecologia 92:317–326

    Google Scholar 

  • Johnston AM, Raven JA, Beardall J, Leegood RC (2001) Photosynthesis in a marine diatom. Nature 112:40–41

    Google Scholar 

  • Kaplan A, Reinhold LL (1999) CO2 concentrating mechanism in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Molr Biol 50:339–370

    Google Scholar 

  • Koch M, Bowes G, Ross C, Zhang X-H (2013) Climate change and ocean.acidification effects on seagrasses and marine macroalgae. Global Change Biol 19:103–132

    Google Scholar 

  • Kroth PG, Chiovitti A, Gruber A, Martin-Jezequel V, Mock T, Parker MS, Stanley MS, Kaplan A, Caron L, Webert T, Maheswari U, Armbrust EV, Bowler C (2008) A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS One 3(1):e1426. doi:10.1371/journal.pone.0001426

    PubMed Central  PubMed  Google Scholar 

  • Long SP (1999) Environmental responses. In: Sage RF, Monson RK (eds) C4 Plant Biology. Academic Press, San Diego, pp 215–249

    Google Scholar 

  • Losh JL, Young JN, Morel FMM (2013) Rubisco is a small fraction of total protein in marine phytoplankton. New Phytol 198:52–58

    CAS  PubMed  Google Scholar 

  • Lucas WJ (1985) Photosynthetic assimilation of exogenous HCO3 − by aquatic plants. Annu Rev Plant Physiol 34:71–104

    Google Scholar 

  • Lucas WJ, Keifer DW, Sanders D (1983) Bicarbonate transport in Chara coralline: evidence for cotransport of HCO3 − with H+. J Membr Biol 73:163–274

    Google Scholar 

  • Lüning K, Dring MJ (1995) Action spectra and spectral quantum yield in marine macroalgae with thin and thick thalli. Mar Biol 87:119–129

    Google Scholar 

  • Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26:439–449

    CAS  Google Scholar 

  • Maberly SC, Madsen TV (2002) Freshwater angiosperms carbon concentrating mechanisms: processes and patterns. Funct Plant Biol 29:393–405

    CAS  Google Scholar 

  • Maberly SC, Raven JA, Johnston AM (1992) Discrimination between 12C and 13C by marine plants. Oecologia 91:481–492

    Google Scholar 

  • Månsson BÅ, McGlade JM (1993) Ecology, thermodynamics and H T Odum’s conjectures. Oecologia 93:582–596

    Google Scholar 

  • Marconi M, Giordano M, Raven JA (2011) Impact of taxonomy, geography and depth on the δ13C and δ15N variation in a large collection of macroalgae. J Phycol 47:1023–1035. doi:10.1111/j.1529-8817.2011.01045.x

    Google Scholar 

  • Markager S (1993) Light absorption and quantum yield for growth in five species of marine macroalgae. J Phycol 29:54–63

    Google Scholar 

  • McGinn PJ, Morel FMM (2008) Expression and inhibition of the carboxylation and decarboxylation enzymes in the photosynthetic C4 pathway of marine diatoms. Plant Physiol 146:300–309

    CAS  PubMed Central  PubMed  Google Scholar 

  • Meyer M, Griffiths H (2013) Origins and diversity of eukaryotic CO2-concentrating mechanisms: lessons for the future. J Exp Bot 64:769–796

    CAS  PubMed  Google Scholar 

  • Miedena M, Prins HBA (1993) Simulation of the light-induced oscillation of the membrane potential in Potamogeton leaf cells. J Membr Biol 133:107–117

    Google Scholar 

  • Morel FMM, Cox EH, Kaepiel AML, Lane TW, Milligan AJ, Schapendoth I, Reinfelder RJ, Tortell PD (2002) Inorganic carbon acquisition by the marine diatom Thalsassiosira weissflogii. Funct Plant Biol 29:301–308. doi:10.1071/PP01199

    CAS  Google Scholar 

  • Moroney JV, Ynalvez RA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6:1251–1259

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moroney JV, Ma Y, Frey WP, Fusilier KP, Pham TT, Simms TA, DiMario RJ, Yang J, Mukerjee B (2011) The carbonic anhydrases of Chlamydomonas reinhardtii: intracellular location, expression and physiological roles. Photosynth Res 109:133–150

    CAS  PubMed  Google Scholar 

  • Moulin P, Andria JR, Axelsson L, Mercado JM (2011) Different mechanisms of inorganic carbon acquisition in red macroalgae (Rhodophyta) revealed by the use of TRIS buffer. Aquatic Bot 95:31–38

    CAS  Google Scholar 

  • Odum HT, Pinkerton RC (1955) Time’s speed regulator: the optimum efficiency for maximum output in physical and biological systems. Am Sci 43:52–58

    Google Scholar 

  • Ogawa T, Kaplan A (2003) Inorganic carbon acquisition mechanism in cyanobacteria. Photosynth Res 77:105–115

    CAS  PubMed  Google Scholar 

  • Patten BC (1993) Toward a more holistic ecology, and science: the contributions of H T Odum. Oecologia 93:597–602

    Google Scholar 

  • Patten BC (1995) Mansson & McGlade vs. H T Odum: a further clarification. Oecologia 95:448

    Google Scholar 

  • Petersen J, Förster K, Turina P, Gräber P (2012) Comparison of the H+/ATP ratios of the H+-ATP synthases from yeast and from chloroplasts. Proc Natl Acad Sci USA 109:11150–11155. doi:10.1073/pnas.1292799109

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pogoryelov D, Klyszejko AL, Krasnoselska GO, Heller E-M, Leone V, Langer JD, Vonck J, Müller DJ, Faraldo-Gómez JD, Meier T (2012) Engineering rotor ring stoichiometries in the ATP synthase. Proc Natnl Acad Sci USA 109:E1599–E1608. doi:10.1073/pnas.1120027/109

    CAS  Google Scholar 

  • Price DG, Badger MR (1985) Inhibition by proton buffers of photosynthetic utilization of bicarbonate by Chara corallina. Austral J Plant Physiol 12:257–267

    CAS  Google Scholar 

  • Price GD, Badger MR, Bassett ME, Whitecross MI (1985) Involvement of plasmalemmasomes and carbonic anhydrase in photosynthyetic utilization of bicarbonate in Chara corallina. Austral J Plant Physiol 12:241–256

    CAS  Google Scholar 

  • Ratti S, Giordano M, Morse D (2007) CO2-concentrating mechanism of the potentially toxic dinoflagellate Protoceratium reticulatum (Dinophyceae, Gonyaulacales). J Phycol 543:693–701

    Google Scholar 

  • Raven JA (1984) Energetics and transport in aquatic plants. A. R, Liss, New York

    Google Scholar 

  • Raven JA (1991) Physiology of inorganic C acquisition and implications for resource used efficiency by marine phytoplankton—relation to increased CO2 and temperature. Plant Cell Environm 14:79–794

    Google Scholar 

  • Raven JA (1997) CO2 concentrating mechanisms: a direct role for thylakoid lumen acidification? Plant Cell Environ 20:147–154

    CAS  Google Scholar 

  • Raven JA (1998) Small is beautiful: the picophytoplankton. Funct Ecol 12:503–513

    Google Scholar 

  • Raven JA (2010) Inorganic carbon acquisition by eukaryotic algae: four current questions. Photosynth Res 106:123–134. doi:10.1007/s11120-010-9563-7

    CAS  PubMed  Google Scholar 

  • Raven JA (2011) The cost of photoinhibition. Physiol Plant 142:87–104. doi:10.1111/j.1399-3054.2011.01465.x

    CAS  PubMed  Google Scholar 

  • Raven JA (2012) Protein turnover and plant RNA and phosphorus requirements in relation to nitrogen fixation. Plant Sci 188–189:25–35. doi:10.1016/j.plantsci.2012.02.010

    PubMed  Google Scholar 

  • Raven JA (2013a) Rubisco: still the most abundant protein on Earth? New Phytol 198:1–3

    CAS  PubMed  Google Scholar 

  • Raven JA (2013b) Half a century of pursuing the pervasive proton. In: Lüttge U et al (eds) Progress in botany, vol 74. Springer, Berlin, pp 3–34

    Google Scholar 

  • Raven JA (2013c) The evolution autotrophy in relation to phosphorus requirements. J Exp Bot 64:4023–4026

    CAS  PubMed  Google Scholar 

  • Raven JA, Glidewell SM (1981) Processes limiting photosynthetic conductance. In: Johnson CB (ed) Physiological processes limiting plant productivity. Butterworths, London, pp 109–136

    Google Scholar 

  • Raven JA, Hurd CJ (2012) Ecophysiology of photosynthesis in macroalgae. Photosynth Res 113:105–125

    CAS  PubMed  Google Scholar 

  • Raven JA, Lucas WJ (1985) The energetics of carbon acquisition. In: Lucas WJ, Berry JA (eds) Inorganic carbon uptake by aquatic photosynthetic organisms. American Society of Plant Physiologists, Rockville, pp 305–324

    Google Scholar 

  • Raven JA, Kübler JI, Beardall J (2000) Put out the light, and then put out the light. J Mar Biol Assoc UK 80:1–25

    CAS  Google Scholar 

  • Raven JA, Johnston AM, Kübler JE, Korb RE, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredricksen J, Dunton KH (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378

    CAS  Google Scholar 

  • Raven JA, Beardall J, Giordano M, Maberly SC (2011) Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynth Res 109:281–296. doi:10.1007/s11120-011-3632-6

    CAS  PubMed  Google Scholar 

  • Raven JA, Beardall J, Giordano M, Maberly SC (2012) Algal evolution in relation to atmospheric CO2: carboxylases, carbon concentrating mechanisms and carbon oxidation cycles. Phil Trans Roy Soc Lond B 367(1588):493–507

    CAS  Google Scholar 

  • Ray S, Klenell M, Choo KS, Pedersen M, Soejis P (2003) Carbon acquisition mechanisms in Chara tomentosa. Aquat Bot 76:141–154

    CAS  Google Scholar 

  • Reinfelder JR (2011) Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu Rev Mar Sci 3:291–395

    Google Scholar 

  • Reinfelder JR, Kraepiel AML, Morel FM (2000) Unicellular C4 photosynthesis in a marine diatom. Nature 407:996–999

    CAS  PubMed  Google Scholar 

  • Reinfelder JR, Milligan AJ, Morel FMM (2004) The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiol 135:2106–2111. doi:10.1104/pp14.041319

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reiskind JB, Bowes G (1991) The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic metabolism. Proc Natl Acad Sci USA 88:2883–2887

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reiskind JB, Seamon PT, Bowes G (1988) Alternative modes of photosynthetic carbon assimilation in marine macroalgae. Plant Physiol 87:686–692

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rexroth S, Mullineaux CW, Ellinger D, Sendtko E, Rōgner M, Koenig F (2011) The plasma membrane of the cyanobacterium Glooeobacter violaceous contains segregated bioenergetic domains. Plant Cell 23:2379–2390

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ritchie RJ, Nadolny C, Larkum AWD (1996) Driving forces for bicarbonate transport in the cyanobacterium Synechococcus R-2 (PCC 7924). Plant Physiol 112:1573–1584

    CAS  PubMed Central  PubMed  Google Scholar 

  • Roberts K, Granum E, Leegood RC, Raven JA (2007a) C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiol 145:230–235. doi:10.1104/pp.107.102616

    CAS  PubMed Central  PubMed  Google Scholar 

  • Roberts K, Granum E, Leegood RC, Raven JA (2007b) Carbon acquisition by diatoms. Phtosynth Res 93:79–88. doi:10.1007/s11120-007-9172-2

    Google Scholar 

  • Sage RF (2013) Stopping the leaks: new insights into C4 photosynthesis at low light. Plant Cell Environ. doi:10.1111/pce.12246

    PubMed  Google Scholar 

  • Sage RF, Zhu X-G (2011) Exploiting the engine of C4 photosynthesis. J Exp Bot 62:2989–3000

    CAS  PubMed  Google Scholar 

  • Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annu Rev Plant Biol 63:19–47

    CAS  PubMed  Google Scholar 

  • Santillán M, Aruas-Hernández LA, Angulo-Brown F (1997) Some optimisation criteria for biological systems in linear irreversible thermodynamics. Il Nuovo Cimento 19:99–109

    Google Scholar 

  • Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimaogama M, Fukuzawa H, Kaplan A, Ogawa T (2002) Genes essential for sodium-dependent bicarbonate transport in cyanobacteria. function and phylogenetic analysis. J Biol Chem 277:18588–18664

    Google Scholar 

  • Smith FA (1985) Historical perspective on HCO3 − assimilation. In: Lucas WJ, Berry JA (eds) Inorganic carbon uptake by aquatic photosynthetic organisms. American Society of Plant Physiologists, Rockville, pp 1–15

    Google Scholar 

  • Spalding MH (2008) Microalagal carbon-dioxide-concentrating mechanisms: Chlamydomonas inorganic carbon transporters. J Exp Bot 59:1463–1473. doi:10.1093/jxb/erm128

    CAS  PubMed  Google Scholar 

  • Tcherkez GGB, Farquhar GD, Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimised. Proc Natl Acad Sci USA 103:7246–7251

    Google Scholar 

  • Uemura K, Awanuzzama, Miyachi S, Yokota A (1997) Ribulose-1, 5-bisphosphate carboxylase–oxygenase from thermophilic red algaewith a strong specifity for CO2 fixation. Biochem Biophys Res Commun 233(2):568–571

  • Walker NA, Smith FA, Cathers IR (1980) Bicarbonate assimilation by freshwater charophytes and higher plants: I membrane transport of bicarbonate ions is not proven. J Membr Biol 57:51–58

    CAS  Google Scholar 

  • Wang Y, Dunamu D, Spalding MH (2011) Carbon concentrating mechanism in Chlamydomonas reinhardtii: inorganic carbon transport and CO2 recapture. Phtosynth Res 109:115–122

    CAS  Google Scholar 

  • Welschmeyer WA, Lorenzen CK (1981) Chlorophyll-specific photosynthesis and quantum efficiency at subsaturating light intensities. J Phycol 36:563–579

    Google Scholar 

  • Wikström M, Hummer G (2012) Stoichiometry of proton translocation by respiratory complex I and its mechanistic implications. Proc Natl Acad Sci USA 109:1431–1436. doi:10.1073/pnas.1120949109

    Google Scholar 

Download references

Acknowledgments

JAR acknowledges helpful discussions with Murray Badger, George Briggs, Paul Falkowski, Richard Geider, Aaron Kaplan, Janet Kübler, Enid MacRobbie, Bruce Osborne, Dean Price. Andrew Smith and Alan Walker. Comments from two anonymous reviewers have been very useful in revising the manuscript. The University of Dundee is a registered Scottish Charity, No 015096,.

Author information

Authors and Affiliations

  1. Division of Plant Science, University of Dundee at the James Hutton Institute, Invergowrie, Dundee, DD2 5DQ, UK

    John A. Raven

  2. Functional Plant Biology and Climate Change Cluster, University of Technology Sydney, Ultimo, NSW, 2007, Australia

    John A. Raven

  3. School of Biological Sciences, Monash University, Clayton, VIC, 3800, Australia

    John Beardall

  4. Department of Marine Science, Università Politecnica Delle Marche, 60131, Ancona, Italy

    Mario Giordano

  5. Institute on Microbiology, ASCR, Algatech, 37981, Trebon, Czech Republic

    Mario Giordano

Authors
  1. John A. Raven
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John Beardall
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mario Giordano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John A. Raven.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Raven, J.A., Beardall, J. & Giordano, M. Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms. Photosynth Res 121, 111–124 (2014). https://doi.org/10.1007/s11120-013-9962-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-013-9962-7

Keywords

Search

Navigation