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Inorganic carbon concentrating mechanisms in relation to the biology of algae

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Abstract

Significant advances have recently been made in our understanding of the mechanism of inorganic carbon transport in algae and, especially, cyanobacteria with inorganic carbon concentrating mechanisms (CCMs). Furthermore, the role of CCMs in increasing the rate of photosynthesis in air-equilibrated solutions is also quite well understood. However, less often considered is how the presence (or absence) of a CCM relates to the biology of algae. This mini-review relates the occurrence of algal CCMs to phylogeny, life form, life history, and interactions with other organisms. While some patterns can be seen, the occurrence of CCMs in relation to the overall biology of the algae needs more investigation.

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References

  • Agusti S, Enriquez S, Frost-Christensen H, Sand-Jensen K and Duarte cm (1994) Light-harvesting among photosynthetic organisms. Funct Ecol 8: 273–279

    Article  Google Scholar 

  • Allen JF and Raven JA (1996) Free radical-induced mutation vs redox regulation: costs and benefits of genes in organelles? JMol Evol 42: 482–492

    Article  CAS  Google Scholar 

  • Andrews M, Box R, Fyson A and Raven JA (1984a) Source-sink characteristics of carbon transport in Chara hispida. Plant Cell Environ 7: 683–687

    CAS  Google Scholar 

  • Andrews M, Davison IR, Andrews ME and Raven JA (1984b) Growth of Chara hispida. I. Apical growth and basal decay. J Ecol 72: 873–884

    Article  Google Scholar 

  • Andrews M, Box R, McInroy S and Raven JA (1984c) Growth of Chara hispida. IIShade adaptation. J Ecol 72: 885–895

    Article  Google Scholar 

  • Atkinson MJ and Smith SV (1983) C:N:P ratios of benthic marine plants. Limnol Oceanogr 28: 568–574

    CAS  Google Scholar 

  • Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W and Price GD (1998) The diversity and co-evolution of Rubisco, plastids, pyrenoids and chloroplast-based CCMs in the algae. Can J Bot 117: 1052–1071

    Article  Google Scholar 

  • Badger MR, Hanson D and Price GD (2002) Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Funct Plant Biol 29: 161–173

    Article  CAS  Google Scholar 

  • Badour SS (1981) The inorganic carbon requirements of Chlamydomonas segnis (Chlorophyceae) for cell-development in synchronous cultures. J Phycol 17: 293–299

    Article  CAS  Google Scholar 

  • Bartlett R and Willey R (1998) Epibiosis of Colacium on Daphnia. Symbiosis 25: 291–299

    Google Scholar 

  • Bates NR, Michaels AF and Knap AH (1996) Seasonal and interannual variability of oceanic carbon dioxide species at the US JGOFS Bermuda Atlantic Time-series Study (BATS) site. Deep-Sea Res II-Topical Stud Oceanogr 43: 347–358

    Article  CAS  Google Scholar 

  • Bates NR, Hansell DA, Carlson CA and Gordon LI (1998) Distribution of CO2 species, estimates of net community production, and air-sea CO2 exchange in the Ross Sea polynya. J Geophys Res Oceans 103(C2): 2883–2896

    Article  CAS  Google Scholar 

  • Beach KS and Smith CM (1996a) Ecophysiology of tropical rhodophytes. 1. Microscale acclimation in pigmentation. J Phycol 32: 701–710

    Article  CAS  Google Scholar 

  • Beach KS and Smith CM (1996b) Ecophysiology of tropical rhodophytes. 2.Microscale acclimation in photosynthesis. J Phycol 32: 710–718

    Article  Google Scholar 

  • Beach KS, Smith CM, Michael T and Shin HW (1995) Photosynthesis in reproductive cells of Ulva fasciata and Enteromorpha flexuosa - implications for ecological success. Mar Ecol Prog Ser 125: 229–237

    Google Scholar 

  • Beardall J and Giordano M (2002) Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation. Funct Plant Biol 29: 335–347

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bell G (1997) The evolution of the life cycle of brown seaweeds. Biol J Linn Soc 60: 21–38

    Article  Google Scholar 

  • Bell G and Mooers AO (1997) Size and complexity among multicellular organisms. Biol J Linn Soc 60: 345–363

    Article  Google Scholar 

  • Box RJ (1986) Quantitative short-term uptake of inorganic phosphate by the Chara hispida rhizoid: short communication. Plant Cell Environ 9: 501–506

    Article  CAS  Google Scholar 

  • Box RJ (1987) The uptake of nitrate and ammonium nitrogen in Chara hispida L. - the contribution of the rhizoid. Plant Cell Environ 10: 169–176

    CAS  Google Scholar 

  • Box RJ (1988) Preliminary comparisons of dry-weight increase with short-term uptake of C, N and P in cultured Chara hispida plants. Bioch Physiol Pflanzen 183: 503–507

    CAS  Google Scholar 

  • Box R, Andrews M and Raven JA (1984) Intercellular transport and cytoplasmic streaming in Chara hispida. J Exp Bot 35: 1016–1021

    Google Scholar 

  • Brostrom G (1998) A note on the C/N and C/P ratio of the biological production in the Nordic seas. Tellus B-Chem Phys Meteorel 50: 93–109

    Article  Google Scholar 

  • Bulte L and Wollman FA (1992) Evidence for a selective downregulation of an integral membrane-protein, the cytochrome b 6/f complex, during gametogenesis in Chlamydomonas reinhardtii. Eur Biochem 204: 327–336

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Calvert HE, Dawes CJ and Borowitzka MA (1976) Phylogenetic relationships of Caulerpa (Chlorophyta) based on comparative chloroplast ultrastructure. J Phycol 12: 149–162

    Article  Google Scholar 

  • Carcino JM, Munoz J, Munoz M and Orellana MC (1987) Effects of the bryozoan Membranipora tuberculata (Bosc.) on the photosynthesis and growth of Gelidium rex. Santelices et Abbot. J Exp Biol 113: 105–112

    Article  Google Scholar 

  • Cavalier-Smith T (2002a) The phagotrophic origin of eukaryotes and the phylogenetic classification of the Protozoa. Int J Syst Evol Microbiol 52: 297–354

    PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2002b) Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr Biol 12: R62–R64

    Article  PubMed  CAS  Google Scholar 

  • Chisholm JRM, Douga C, Ageron E and Gimont PAD (1996) 'Roots' in mixotrophic algae. Nature 381: 382

    Article  CAS  Google Scholar 

  • Clayton MN (1990) Phaeophyta. In: Clayton MN and King RJ (eds) Biology of Marine Plants, pp 149-182. Longman Cheshire, Melbourne

    Google Scholar 

  • Codispoti LA, Friederich GE, Iverson RL and Hood DW (1982) Temporal changes in the inorganic carbon system of the southeastern Bering Sea during spring 1980. Nature 296: 242–245

    Article  CAS  Google Scholar 

  • Codispoti LA, Friederich GE and Hood DW (1986) Variability in the inorganic carbon system over the southeastern Bering Sea Shelf during spring 1980 and spring summer 1981. Cont Shelf Res 5: 133–160

    Article  Google Scholar 

  • Cole JJ, Caraco NF, Kling GW and Kratz TK (1994) Carbon dioxide supersaturation in the surface waters of lakes. Science 265: 1568–1570

    CAS  PubMed  Google Scholar 

  • Colman B, Huertos IE, Bhatti S and Dason JS (2002) The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae. Funct Plant Biol 29: 261–270

    Article  CAS  Google Scholar 

  • Cowan IK, Lange OL and Green TGA (1992) Carbon-dioxide exchange in lichens - determination of transport and carboxylation characteristics. Planta 187: 282–294

    Article  CAS  Google Scholar 

  • Creed JC, Norton TA and Kain JM (1997) Intraspecific competition in Fucus serratus germlings: the interaction of light, nutrients and density. J Exp Mar Biol Ecol 212: 211–223

    Article  Google Scholar 

  • Davy SK, Trautman DA, Borowitzka MA and Hinde R (2002) Ammonium excretion by a symbiotic sponge supplies the nitrogen requirements of its rhodophyte partner. J Exp Biol 205: 3505–3511

    PubMed  CAS  Google Scholar 

  • Douglas AE and Raven JA (2003) Genomes at the interface between bacteria and organelles. Phil Trans R Soc London B 358: 5–18

    Article  CAS  Google Scholar 

  • Duarte CM (1992) Nutrient concentration of aquatic plants - patterns across species. Limnol Oceanogr 37: 882–889

    CAS  Google Scholar 

  • Duarte CM, Sand-Jensen K, Nielsen SL, Enriquez S and Agusti S (1995) Comparative functional plant ecology - rationale and potentials. Trends Ecol Evol 10: 418–421

    Article  Google Scholar 

  • Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotirer JB, Harrison JF, Hobbie SE, Odell GM and Weider LJ (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3: 540–550

    Article  Google Scholar 

  • Enriquez S, Duarte CM, Sand-Jensen K and Nielsen SL (1996) Broad-scale comparison of photosynthetic rates across phototrophic organisms. Oecologia 108: 197–206

    Google Scholar 

  • Evans LV (1968) Chloroplast morphology and fine structure in British fucoids. New Phytol 67: 173–178

    Article  Google Scholar 

  • Falkowski PG (1997) The paradox of carbon dioxide efflux. Curr Biol 7: R637–639

    Article  PubMed  CAS  Google Scholar 

  • Falkowski PG (2000) Rationalizing elemental ratios in unicellular algae. J Phycol 36: 3–6

    Article  CAS  Google Scholar 

  • Falkowski PG and Raven JA (1997) Aquatic Photosynthesis. Blackwell Science, Malden, Massachusetts

    Google Scholar 

  • Famà P, Wyser B, Kooistra WHCF and Zuccarello GC (2002) Molecular phylogeny of the genus Caulerpa (Caulerpales, Chlorophyta) inferred from chloroplast tufA gene. J Phycol 38: 1040–1050

    Article  Google Scholar 

  • Geider RJ and La Roche J (2002) Redfield revisited: Variability of C:N:P in marine microalgae and its biochemical basis. Eur J Phycol 37: 1–17

    Article  Google Scholar 

  • Graham LE and Wilcox LW (2000) Algae. Prentice-Hall, Upper Saddle River, New Jersey

    Google Scholar 

  • Haxo FT and Clendinning KA (1953) Photosynthesis and phototoxis in Ulva lactuca gametes. Biol Bull 103: 103–114

    Google Scholar 

  • Hein M and Sand-Jensen K (1997) CO2 increases oceanic primary production. Nature 388: 526–527

    Article  CAS  Google Scholar 

  • Hein M, Pedersen MF and Sand-Jensen K (1995) Size-dependent nitrogen uptake in micro-and macro-algae. Mar Ecol Progr Ser 118: 247–253

    Google Scholar 

  • Hemminga MA and Duarte CM (2000) Seagrass Ecology. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Hess WR, Rocap G, Ting CS, Larimer F, Stilwagen S, Lamerdin J and Chisholm SW (2001) The photosynthetic apparatus of Prochlorococcus: Insights through comparative genomics Photosynth Res 70: 53–71

    CAS  Google Scholar 

  • Honneger R and Peter M (1994) Routes of solute retranslocation and the location of water in heteromerous lichens visualized with cryotechniques in light and electron-microscopy. Symbiosis 16: 167–186

    Google Scholar 

  • Huertas IE, Espie GS, Colman B and Lubian LM (2000) Lightdependent bicarbonate uptake and CO2 efflux in the marine microalga Nannochloropsis gaditana. Planta 211: 43–49

    Article  PubMed  CAS  Google Scholar 

  • Huertas IE, Colman B and Espie GS (2002) Inorganic carbon acquisition and its energization in eustigmatophyte algae. Funct Plant Biol 29: 271–277

    Article  CAS  Google Scholar 

  • Hurd CL (2000) Water motion, marine macroalgal physiology, and production. J Phycol 36: 453–472

    Article  CAS  Google Scholar 

  • Hurd CL, Duarte KM, Chia FS and Harrison PJ (1994) Effect of bryozoan colonization on inorganic nitrogen acquisition by the kelps Agarum fimbriatum and Mactocystis integrifolia. Mar Biol 121: 167–173

    Article  Google Scholar 

  • Hurd CL, Duarte KM and Harrison PJ (2000) Influence of bryozoan calorization on the physiology of the kelp Macrocystis integrifolia (Laminariales, Phaeophyta) from nitrogen-rich and-poor sites in Barkley Sound, British Columbia, Canada. Phycologia 39: 435–440

    Article  Google Scholar 

  • Jacquelt S, Prieur L, Avois-Jacquet C, Lennon J-F and Vaulot D (2002) Short-timescale variability of picophytoplankton abundance and cellular parameters in surface waters of the Alboran Sea (western Mediterranean). J Plankton Res 24: 635–651

    Article  Google Scholar 

  • Jorgensen BB and Des Marais DJ (1990) The diffusive boundary layer of sediments: Oxygen microgradients over a microbial mat. Limnol Oceanogr 35: 1343–1355

    PubMed  CAS  Google Scholar 

  • Kain JM (1969) The biology of Laminaria hyperborea. V. Comparison with the early stages of competitors. J Mar Biol Assoc UK 49: 455–473

    Google Scholar 

  • Kaplan A and Reinhold L (1999) CO2 concentrating mechanisms in photosynthetic microorganisms. Ann Rev Plant Physiol Plant Mol Biol 50: 539–570

    Article  CAS  Google Scholar 

  • Kirk DL (1998) Volvox. Molecular-genetic origins of multicellularity and cellular differentiation. Cambridge University Press, Cambridge, UK [see also review by Raven JA (1999) Eur J Phycol 33: 275-278]

    Google Scholar 

  • Krupinska K and Humbeck K (1994) Light-induced synchronous cultures, an excellent tool to study the cell-cycle of unicellular green algae. J Photochem Photobiol B - Biol 26: 217–231

    Article  CAS  Google Scholar 

  • Lagus A and Lindholm T (2000) Occurrence of the euglenoid epibiont Colacium sp., on the rotifer Keratella cochlearis Gesse in coastal inlets in Aland, SW Finland. Arch Hydrobiol 149: 489–500

    Google Scholar 

  • Lawlor DW (2001) Photosynthesis: Molecular, Physiological and Environmental Processes. Springer-Verlag, Berlin

    Google Scholar 

  • Leggat W, Marendy EM, Baillie B, Whitney SM, Ludwig M, Badger MR and Yellowlees D (2002) Dinoflagellate symbioses: strategies and adaptations for the acquisition and fixation of inorganic carbon. Funct Plant Biol 29: 309–322

    Article  CAS  Google Scholar 

  • Leukart P and Lüning K (1994) Minimum spectral light requirements and maximal light levels for long-term germling growth of several red algae from different water depths and a green alga. Eur J Phycol 29: 103–112

    Google Scholar 

  • Lüning K (1990) Seaweeds, Their Environment, Biogeography and Ecophysiology. John Wiley, New York

    Google Scholar 

  • Luther H (1949) Vorschlag zu einer Ökologischen Grundeinleitung der Hydrophyten. Acta Bot Fenn 44: 1–15

    Google Scholar 

  • Maberly SC (1996) Diel, episodic and seasonal changes in pH and concentration of inorganic carbon in a productive lake. Freshwater Biol 35: 579–598

    Article  CAS  Google Scholar 

  • Maranger R, Bird DF and Price NM (1990) Iron acquisition by photosynthetic marine phytoplankton from ingested bacteria. Nature 396: 248–251

    Google Scholar 

  • Marcus Y, Schuster G, Michaels A and Kaplan A (1986) Adaptation to CO2 levels and changes in the phosphorylation of thylakoid proteins during the cell-cycle of Chlamydomonas reinhardtii. Plant Physiol 80: 604–607

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Rujan T, Richly E, Hansen A, Cornelsen S., Lins T, Leister D, Stoebe W, Hasegawa M and Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial and chloroplast genomes reveals plastid phyologeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99: 12246–12251.

    Article  PubMed  CAS  Google Scholar 

  • Matsuda Y, Satoh K, Hanada H, Satch D, Hiraoka Y and Hand T (2002) Regulation of the expressions of HCO3¯uptake and intracellular carbonic anhydrase in response to CO2 concentration in the marine diatom Phaeodactylum sp. Funct Plant Biol 29: 279–287

    Article  CAS  Google Scholar 

  • McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J Phycol 37: 951–959

    Article  Google Scholar 

  • McLachlan J and Bidwell RGS (1978) Photosynthesis of eggs, sperm, zygotes and embryos of Fucus serratus. Can J Bot 56: 371–373

    CAS  Google Scholar 

  • Mercado JM, Carmona R and Niell FX (1998) Bryozoans increase available CO2 for photosynthesis in Gelidium sesquipedale (Rhodophyceae). J Phycol 36: 925–927

    Article  Google Scholar 

  • Mercado JM, Niell FX and Gil-Rodriguez MC (2001) Photosynthesis might be limited by light, not inorganic carbon availability, in three intertidal Gelidium species. New Phytol 149: 431–439

    Article  CAS  Google Scholar 

  • Morel FMM, Cox EM, Kraepiel AML, Lane TW, Milligan AJ, Schapendoth I, Reinfelder JR and Tortell PD (2002) Acquisition of inorganic carbon by the marine diatom Thalassiosira weissflogii. Funct Plant Biol 29: 301–308

    Article  CAS  Google Scholar 

  • Morita E, Abe T, Tsuzuki M, Fujiwana S, Sato N, Hirata A, Sonoike K and Nozaki H (1998) Presence of CO2 concentrating mechanisms in some pyrenoid-less free-living algal genes Chloromonas (Volvocale, Chlorophyta). Planta 204: 269–276

    Article  PubMed  CAS  Google Scholar 

  • Morita E, Abe T, Tsuzuki M, Fujiana S, Sato N, Hirata A, Sonoike K and 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

    Article  Google Scholar 

  • Moroney JV and Somarchi A (1999) How do alga concentrate CO2 to increase the efficiency of photosynthetic carbon fixation. Plant Physiol 89: 897–903

    Google Scholar 

  • Munoz J, Carcino JM and Molina MX (1991) Effect of encrusting bryozoans on the physiology of their algal substratum. J Mar Biol Assoc UK 71: 877–882

    Article  Google Scholar 

  • Neilsen SL, Enriquez S, Duarte CM and Sand-Jensen K (1996) Scaling maximum growth rates across photosynthetic organisms. Funct Ecol 10:167–175

    Article  Google Scholar 

  • Nodwell LM and Price NM (2001) Direct use of inorganic colloidal iron bymarine mixotrophic phytoplankton. Limnol Oceanogr 46: 765–777

    Article  CAS  Google Scholar 

  • Palmqvist K (2000) Carbon economy in lichens. New Phytol 148: 11–36

    Article  CAS  Google Scholar 

  • Palmqvist K, Samuelsson G and Badger MR (1994) Photobiontrelated differences in carbon acquisition among green algal lichens. Planta 195: 70–79.

    Article  CAS  Google Scholar 

  • Pearson GA, Serrao EA and Brawley SH (1998) Control of gamete release in fucoid algae: sensing hydrodynamic conditions via carbon acquisition. Ecology 79: 1725–1739

    Article  Google Scholar 

  • Poole LJ and Raven JA (1997) The Biology of Enteromorpha. Progr Phycol Res 12: 1–148

    CAS  Google Scholar 

  • Purvis OW, Coppins BJ, Hawksworth DL, James PW and Moore DM (eds) (1992) The Lichen Flora of Great Britain and Ireland. Natural History Museum Publications in association with the British Lichen Society, London

    Google Scholar 

  • Raven JA (1970) Exogenous inorganic carbon sources in plant photosynthesis. Biol Rev 45: 167–221

    CAS  Google Scholar 

  • Raven JA (1972) Endogenous inorganic carbon sources in plant photosynthesis. I. Occurrence of the dark respiratory pathways in illuminated green cells. New Phytol 71: 227–247.

    Article  CAS  Google Scholar 

  • Raven JA (1981) Nutritional strategies of submerged benthic plants: The acquisition of C, N and P by rhizophytes and haptophytes. New Phytol 88: 1–30

    Article  CAS  Google Scholar 

  • Raven JA (1982) The energetics of freshwater algae: Energy requirements for biosynthesis and volume regulation. New Phytol 92: 1–20

    Article  Google Scholar 

  • Raven JA (1984) Energetics and Transport in Aquatic Plants. A R Liss, New York

    Google Scholar 

  • Raven JA (1986) Physiological consequences of extremely small size for autotrophic organisms in the sea. In: Platt T and Li WKW (eds) Photosynthetic Picoplankton, pp. 1–70. Can Bull Fish Aquat Sci 214

  • Raven JA (1991) Implications of inorganic C utilization: Ecology, evolution and geochemistry. Can J Plant Physiol 69: 908–924

    CAS  Google Scholar 

  • Raven JA (1993a) The roles of the Chantransia phase of Lemanea (Lemaneaceae, Batrachospermales, Rhodophyta) and of the 'mushroom' phase of Himanthalia (Himanthaliaceae, Fucales, Phaeophyta). Bot J Scot 46: 477–485

    Article  Google Scholar 

  • Raven JA (1993b) Energy and nutrient acquisition by autotrophic symbioses and their asymbiotic ancestors. Symbiosis 14: 33–60

    Google Scholar 

  • Raven JA (1994) Why are there no picoplankton O2 evolvers with volumes less than 10¯19 m3? J Plankton Res 16: 565–580

    Google Scholar 

  • Raven JA (1995) Costs and benefits of low intracellular osmolarity in cells of freshwater algae. Funct Ecol 9: 701–707

    Article  Google Scholar 

  • Raven JA (1997a) Multiple origins of plasmodesmata. Eur J Phycol 32: 95–101

    Article  Google Scholar 

  • Raven JA (1997b) Phagotrophy in phototrophs. Limnol Oceanogr 42: 198–205

    CAS  Google Scholar 

  • Raven JA (1997c) Inorganic carbon acquisition by marine autotrophs. Adv Botan Res 27: 85–209

    CAS  Google Scholar 

  • Raven JA (1997d) Putting the C in phycology. Eur J Phycol 32: 319–333

    Article  Google Scholar 

  • Raven JA (1997e) The vacuole: A cost-benefit analysis. Adv Bot Res 25: 59–86

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Raven JA (1998b) Picophytoplankton. Progr Phycol Res 13: 33–106

    Google Scholar 

  • Raven JA (1999a) The size of cells and organisms in relation to the evolution of embryophytes. Plant Biol 1: 2–12

    Google Scholar 

  • Raven JA (1999b) The flagellate condition. In: Leadbeater BSC and Green JC (eds) The Flagellates: Unity, Diversity and Evolution, pp. 27–48. Taylor and Francis, London

    Google Scholar 

  • Raven JA (2003) Carboxysomes and peptidoglycan walls of cyanelles: possible physiological functions. Eur J Phycol 38: 47–53

    Article  Google Scholar 

  • Raven JA and Falkowski PG (1999) Oceanic sinks for atmospheric CO2. Plant Cell Environ 22: 741–755

    Article  CAS  Google Scholar 

  • Raven JA and Kübler JE (2002) New light on the scaling of metabolic rate with the size of algae. J Phycol 38: 11–16

    Article  Google Scholar 

  • Raven JA and Osmond CB (1992) Inorganic carbon assimilation processes and their ecological significance in inter-and sub-tidal macroalgae of North Carolina. Funct Ecol 6: 41–47

    Article  Google Scholar 

  • Raven JA, Johnston AM, Handley LL and McInroy SG (1990) Transport and assimilation of inorganic carbon by Lichnia pygmaea under emersed and submersed conditions. New Phytol 114: 407–417

    Article  CAS  Google Scholar 

  • Raven JA, Walker DI, Jensen KR, Handley LL, Scrimgeour CM and McInroy SG (2001) What fraction of the organic carbon in sacoglossans is obtained from photosynthesis by kleptoplastids? An investigation using the natural abundance of stable carbon isotopes. Mar Biol 138: 537–545

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Raven JA, Johnston AM, Kübler JE, Korb RE, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Clayton MN, Vanderklift M, Chudek JA, Fredriksen S and Dunton KH (2002b) Seaweeds in cold seas: evolution and carbon acquisition. Ann Bot 90: 525–536

    Article  PubMed  CAS  Google Scholar 

  • Robertson JE, Watson AJ, Langdon C, Ling RD and Wood JW (1993) Diurnal variation in surface pCO2 and O2 60 degrees N, 20 degrees W in the North Atlantic. Deep Sea Res II Top Stud Oceanogr 40: 409–422

    Article  CAS  Google Scholar 

  • Rowat M and Moroney JV (1995) The regulation of carbonic anhydrase and ribulose-1,5-bisphosphate carboxylase oxygenase activase by light and CO2 in Chlamydomonas reinhardtii. Plant Physiol 109: 937–944

    PubMed  Google Scholar 

  • Rujin T and Martin W(2001) How many genes in Arabidopsis come from cyanobacteria? An estimate from 386 protein phylogenies. Trend Genet 17: 113–120

    Article  Google Scholar 

  • Sand-Jensen KAJ (1977) Effects of epiphytes on eelgrass photosynthesis. Aquat Bot 3: 55–63

    Article  CAS  Google Scholar 

  • Sand-Jensen K and Pedersen MF (1994) Photosynthesis by symbiotic algae in the freshwater sponge Spongilla lacustris. Limnol Oceanogr 39: 551–561

    CAS  Google Scholar 

  • Sand-Jensen K, Pedersen O and Geertz-Hansen O (1997) Regulation and role of photosynthesis in the colonial ciliate Ophrydium versatile. Limnol Oceanogr 42: 866–873

    CAS  Google Scholar 

  • Schaffelke B (1999) Particulate matter as an alternative nutrient source for tropical Sargassum species (Fucales, Phaeophyceae). J Phycol 33: 1150–1157

    Article  Google Scholar 

  • Scherrer S, Haish A and Honneger R (2002) Characterization and expression of 7PH1, the hydrophobin gene of the lichen-forming ascomycete Xanthoria parietina. New Phytol 154: 175–184

    Article  CAS  Google Scholar 

  • Serrao EA, Pearson G, Kauksky L and Brawley SH (1996) Successful external fertilization in turbulent conditions. Proc Natl Acad Sci USA 93: 3286–5290

    Article  Google Scholar 

  • Spalding MH, Van K, Wang Y and Nakamura Y (2002) Acclimation of Chlamydomonas to changing carbon availability. Funct Plant Biol 29: 221–230

    Article  CAS  Google Scholar 

  • Speransky SR, Brawley SH and Halteman WA (2000) Gamete release is increased by calm conditions in the coenocytic green alga Bryopsis (Chlorophyta). J Phycol 36: 730–739

    Article  Google Scholar 

  • Sukenik A, Tchernov D, Kaplan A, Huertos E, Lubian LM and Livne A (1997) Uptake, efflux and photosynthetic utilization of inorganic carbon by the marine eustigmatophyte Nannochloropsis sp. J Phycol 33: 969–974

    Article  CAS  Google Scholar 

  • Sweeney C, Smith WO, Hales B, Bidigare RR, Carlson CA, Codispoti LA, Gordon LI, Hansell DA, Millero FJ, Park MO and Takahashi T (2000) Nutrient and carbon removal ratios and fluxes in the Ross Sea, Antarctica. Deep Sea Res II Top Stud Oceanogr 43: 3395–3421

    Article  Google Scholar 

  • Tan CK and Badour SS (1983) Photoassimilation of inorganic carbon in Chlamydomonas segnis during cell development at low and high carbon dioxide tension. Z Pflanzenphysiol 109: 113–125

    CAS  Google Scholar 

  • Tchernov D, Hassidim M, Luz B, Sukenik A, Reinhold L and Kaplan A (1997) Sustained net CO2 evolution during photosynthesis by marine microorganisms. Curr Biol 7: 723–728

    Article  PubMed  CAS  Google Scholar 

  • Thyssen C, Schlichting R and Giersch C (2001) The CO2-concentrating mechanism in the physiological context: lowering the CO2 supply diminishes culture growth and economizes starch utilization in Chlamydomonas reinhardtii. Planta 213: 629–639

    Article  PubMed  CAS  Google Scholar 

  • Thyssen C, van Hunnik E, Navarro MT, Fernandez E, Galván A and Sültemeyer D (2002) Analysis of Chlamydomonas mutants uptake systems. Funct Plant Biol 29: 251–260

    Article  CAS  Google Scholar 

  • Ting CS, Rocap G, King J and Chisholm SW (2002) Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microbial 10: 134–142

    Article  CAS  Google Scholar 

  • Tomitani A, Okada K, Miyashita H, Matthijs HC, Ohno T and Tanaka A (1999) Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature 400: 159–162

    Article  PubMed  CAS  Google Scholar 

  • Tortell PD (2000) Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnol Oceanogr 45: 744–750

    Article  CAS  Google Scholar 

  • Tortell PD, Rau GH and Morel FMM (2000) Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnol Oceanogr 45: 1485–1500

    Article  CAS  Google Scholar 

  • Trembley ML, Ringli C and Honneger R (2002) Differential expression of hydrophorbens DGH1, DGH2 and DGH3 and immunolocalization of DGH1 in strata of the lichenized basidiocarp of Dictyonema glabratum. New Phytol 154: 185–195

    Article  CAS  Google Scholar 

  • Van den Hoek C, Mann DG and Jahns HM (1995) Algae. An Introduction to Phycology. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Watson AJ, Robinson C, Robinson JE, Williams PJL and Fasham MJR (1991) Spatial variability in the sink for atmospheric carbon dioxide in the North Atlantic. Nature 350: 50–53

    Article  CAS  Google Scholar 

  • Williams SL (1984) Uptake of sediment ammonium and translocation in a marine macroalga Caulerpa cupressoides. Limnol Oceanogr 29: 374–379

    Article  CAS  Google Scholar 

  • Williams SL and Fisher TR (1985) Kinetics of nitrogen-15 labelled ammonium uptake by Caulerpa cupressoides (Chlorophyta). J Phycol 21: 287–296

    Article  CAS  Google Scholar 

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  1. Division of Environmental and Applied Biology, School of Life Sciences, University of Dundee, Dundee, DD1 4HN, UK

    John A. Raven

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Raven, J.A. Inorganic carbon concentrating mechanisms in relation to the biology of algae. Photosynthesis Research 77, 155–171 (2003). https://doi.org/10.1023/A:1025877902752

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