Advertisement

Photosynthesis Research

, Volume 77, Issue 2–3, pp 155–171 | Cite as

Inorganic carbon concentrating mechanisms in relation to the biology of algae

  • John A. Raven
Article

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.

algae carbon concentrating mechanism kleptoplastids life cycle life form phagotrophy 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agusti S, Enriquez S, Frost-Christensen H, Sand-Jensen K and Duarte cm (1994) Light-harvesting among photosynthetic organisms. Funct Ecol 8: 273–279CrossRefGoogle Scholar
  2. Allen JF and Raven JA (1996) Free radical-induced mutation vs redox regulation: costs and benefits of genes in organelles? JMol Evol 42: 482–492CrossRefGoogle Scholar
  3. Andrews M, Box R, Fyson A and Raven JA (1984a) Source-sink characteristics of carbon transport in Chara hispida. Plant Cell Environ 7: 683–687Google Scholar
  4. Andrews M, Davison IR, Andrews ME and Raven JA (1984b) Growth of Chara hispida. I. Apical growth and basal decay. J Ecol 72: 873–884CrossRefGoogle Scholar
  5. Andrews M, Box R, McInroy S and Raven JA (1984c) Growth of Chara hispida. IIShade adaptation. J Ecol 72: 885–895CrossRefGoogle Scholar
  6. Atkinson MJ and Smith SV (1983) C:N:P ratios of benthic marine plants. Limnol Oceanogr 28: 568–574Google Scholar
  7. 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: 1052–1071CrossRefGoogle Scholar
  8. Badger MR, Hanson D and Price GD (2002) Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Funct Plant Biol 29: 161–173CrossRefGoogle Scholar
  9. Badour SS (1981) The inorganic carbon requirements of Chlamydomonas segnis (Chlorophyceae) for cell-development in synchronous cultures. J Phycol 17: 293–299CrossRefGoogle Scholar
  10. Bartlett R and Willey R (1998) Epibiosis of Colacium on Daphnia. Symbiosis 25: 291–299Google Scholar
  11. 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: 347–358CrossRefGoogle Scholar
  12. 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): 2883–2896CrossRefGoogle Scholar
  13. Beach KS and Smith CM (1996a) Ecophysiology of tropical rhodophytes. 1. Microscale acclimation in pigmentation. J Phycol 32: 701–710CrossRefGoogle Scholar
  14. Beach KS and Smith CM (1996b) Ecophysiology of tropical rhodophytes. 2.Microscale acclimation in photosynthesis. J Phycol 32: 710–718CrossRefGoogle Scholar
  15. 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: 229–237Google Scholar
  16. Beardall J and Giordano M (2002) Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation. Funct Plant Biol 29: 335–347CrossRefGoogle Scholar
  17. Beer S, Bjork M, Hellblom F and Axelsson L (2002) Inorganic carbon utilization in marine angiosperms (seagrasses). Funct Plant Biol 29: 349–354CrossRefGoogle Scholar
  18. Bell G (1997) The evolution of the life cycle of brown seaweeds. Biol J Linn Soc 60: 21–38CrossRefGoogle Scholar
  19. Bell G and Mooers AO (1997) Size and complexity among multicellular organisms. Biol J Linn Soc 60: 345–363CrossRefGoogle Scholar
  20. Box RJ (1986) Quantitative short-term uptake of inorganic phosphate by the Chara hispida rhizoid: short communication. Plant Cell Environ 9: 501–506CrossRefGoogle Scholar
  21. Box RJ (1987) The uptake of nitrate and ammonium nitrogen in Chara hispida L. - the contribution of the rhizoid. Plant Cell Environ 10: 169–176Google Scholar
  22. 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: 503–507Google Scholar
  23. Box R, Andrews M and Raven JA (1984) Intercellular transport and cytoplasmic streaming in Chara hispida. J Exp Bot 35: 1016–1021Google Scholar
  24. 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: 93–109CrossRefGoogle Scholar
  25. 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: 327–336CrossRefGoogle Scholar
  26. 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: 1378–1391CrossRefGoogle Scholar
  27. Calvert HE, Dawes CJ and Borowitzka MA (1976) Phylogenetic relationships of Caulerpa (Chlorophyta) based on comparative chloroplast ultrastructure. J Phycol 12: 149–162CrossRefGoogle Scholar
  28. 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: 105–112CrossRefGoogle Scholar
  29. Cavalier-Smith T (2002a) The phagotrophic origin of eukaryotes and the phylogenetic classification of the Protozoa. Int J Syst Evol Microbiol 52: 297–354PubMedGoogle Scholar
  30. Cavalier-Smith T (2002b) Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr Biol 12: R62–R64CrossRefPubMedGoogle Scholar
  31. Chisholm JRM, Douga C, Ageron E and Gimont PAD (1996) 'Roots' in mixotrophic algae. Nature 381: 382CrossRefGoogle Scholar
  32. Clayton MN (1990) Phaeophyta. In: Clayton MN and King RJ (eds) Biology of Marine Plants, pp 149-182. Longman Cheshire, MelbourneGoogle Scholar
  33. 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: 242–245CrossRefGoogle Scholar
  34. 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: 133–160CrossRefGoogle Scholar
  35. Cole JJ, Caraco NF, Kling GW and Kratz TK (1994) Carbon dioxide supersaturation in the surface waters of lakes. Science 265: 1568–1570PubMedGoogle Scholar
  36. Colman B, Huertos IE, Bhatti S and Dason JS (2002) The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae. Funct Plant Biol 29: 261–270CrossRefGoogle Scholar
  37. Cowan IK, Lange OL and Green TGA (1992) Carbon-dioxide exchange in lichens - determination of transport and carboxylation characteristics. Planta 187: 282–294CrossRefGoogle Scholar
  38. 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: 211–223CrossRefGoogle Scholar
  39. 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: 3505–3511PubMedGoogle Scholar
  40. Douglas AE and Raven JA (2003) Genomes at the interface between bacteria and organelles. Phil Trans R Soc London B 358: 5–18CrossRefGoogle Scholar
  41. Duarte CM (1992) Nutrient concentration of aquatic plants - patterns across species. Limnol Oceanogr 37: 882–889Google Scholar
  42. Duarte CM, Sand-Jensen K, Nielsen SL, Enriquez S and Agusti S (1995) Comparative functional plant ecology - rationale and potentials. Trends Ecol Evol 10: 418–421CrossRefGoogle Scholar
  43. 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: 540–550CrossRefGoogle Scholar
  44. Enriquez S, Duarte CM, Sand-Jensen K and Nielsen SL (1996) Broad-scale comparison of photosynthetic rates across phototrophic organisms. Oecologia 108: 197–206Google Scholar
  45. Evans LV (1968) Chloroplast morphology and fine structure in British fucoids. New Phytol 67: 173–178CrossRefGoogle Scholar
  46. Falkowski PG (1997) The paradox of carbon dioxide efflux. Curr Biol 7: R637–639CrossRefPubMedGoogle Scholar
  47. Falkowski PG (2000) Rationalizing elemental ratios in unicellular algae. J Phycol 36: 3–6CrossRefGoogle Scholar
  48. Falkowski PG and Raven JA (1997) Aquatic Photosynthesis. Blackwell Science, Malden, MassachusettsGoogle Scholar
  49. 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: 1040–1050CrossRefGoogle Scholar
  50. 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: 1–17CrossRefGoogle Scholar
  51. Graham LE and Wilcox LW (2000) Algae. Prentice-Hall, Upper Saddle River, New JerseyGoogle Scholar
  52. Haxo FT and Clendinning KA (1953) Photosynthesis and phototoxis in Ulva lactuca gametes. Biol Bull 103: 103–114Google Scholar
  53. Hein M and Sand-Jensen K (1997) CO2 increases oceanic primary production. Nature 388: 526–527CrossRefGoogle Scholar
  54. Hein M, Pedersen MF and Sand-Jensen K (1995) Size-dependent nitrogen uptake in micro-and macro-algae. Mar Ecol Progr Ser 118: 247–253Google Scholar
  55. Hemminga MA and Duarte CM (2000) Seagrass Ecology. Cambridge University Press, Cambridge, UKGoogle Scholar
  56. 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: 53–71Google Scholar
  57. 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: 167–186Google Scholar
  58. Huertas IE, Espie GS, Colman B and Lubian LM (2000) Lightdependent bicarbonate uptake and CO2 efflux in the marine microalga Nannochloropsis gaditana. Planta 211: 43–49CrossRefPubMedGoogle Scholar
  59. Huertas IE, Colman B and Espie GS (2002) Inorganic carbon acquisition and its energization in eustigmatophyte algae. Funct Plant Biol 29: 271–277CrossRefGoogle Scholar
  60. Hurd CL (2000) Water motion, marine macroalgal physiology, and production. J Phycol 36: 453–472CrossRefGoogle Scholar
  61. 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: 167–173CrossRefGoogle Scholar
  62. 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: 435–440CrossRefGoogle Scholar
  63. 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: 635–651CrossRefGoogle Scholar
  64. Jorgensen BB and Des Marais DJ (1990) The diffusive boundary layer of sediments: Oxygen microgradients over a microbial mat. Limnol Oceanogr 35: 1343–1355PubMedGoogle Scholar
  65. Kain JM (1969) The biology of Laminaria hyperborea. V. Comparison with the early stages of competitors. J Mar Biol Assoc UK 49: 455–473Google Scholar
  66. Kaplan A and Reinhold L (1999) CO2 concentrating mechanisms in photosynthetic microorganisms. Ann Rev Plant Physiol Plant Mol Biol 50: 539–570CrossRefGoogle Scholar
  67. 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
  68. 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: 217–231CrossRefGoogle Scholar
  69. 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: 489–500Google Scholar
  70. Lawlor DW (2001) Photosynthesis: Molecular, Physiological and Environmental Processes. Springer-Verlag, BerlinGoogle Scholar
  71. 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: 309–322CrossRefGoogle Scholar
  72. 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: 103–112Google Scholar
  73. Lüning K (1990) Seaweeds, Their Environment, Biogeography and Ecophysiology. John Wiley, New YorkGoogle Scholar
  74. Luther H (1949) Vorschlag zu einer Ökologischen Grundeinleitung der Hydrophyten. Acta Bot Fenn 44: 1–15Google Scholar
  75. Maberly SC (1996) Diel, episodic and seasonal changes in pH and concentration of inorganic carbon in a productive lake. Freshwater Biol 35: 579–598CrossRefGoogle Scholar
  76. Maranger R, Bird DF and Price NM (1990) Iron acquisition by photosynthetic marine phytoplankton from ingested bacteria. Nature 396: 248–251Google Scholar
  77. 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: 604–607PubMedCrossRefGoogle Scholar
  78. 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.CrossRefPubMedGoogle Scholar
  79. 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: 279–287CrossRefGoogle Scholar
  80. McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J Phycol 37: 951–959CrossRefGoogle Scholar
  81. McLachlan J and Bidwell RGS (1978) Photosynthesis of eggs, sperm, zygotes and embryos of Fucus serratus. Can J Bot 56: 371–373Google Scholar
  82. Mercado JM, Carmona R and Niell FX (1998) Bryozoans increase available CO2 for photosynthesis in Gelidium sesquipedale (Rhodophyceae). J Phycol 36: 925–927CrossRefGoogle Scholar
  83. 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: 431–439CrossRefGoogle Scholar
  84. 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: 301–308CrossRefGoogle Scholar
  85. 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: 269–276CrossRefPubMedGoogle Scholar
  86. 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: 365–372CrossRefGoogle Scholar
  87. Moroney JV and Somarchi A (1999) How do alga concentrate CO2 to increase the efficiency of photosynthetic carbon fixation. Plant Physiol 89: 897–903Google Scholar
  88. 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: 877–882CrossRefGoogle Scholar
  89. Neilsen SL, Enriquez S, Duarte CM and Sand-Jensen K (1996) Scaling maximum growth rates across photosynthetic organisms. Funct Ecol 10:167–175CrossRefGoogle Scholar
  90. Nodwell LM and Price NM (2001) Direct use of inorganic colloidal iron bymarine mixotrophic phytoplankton. Limnol Oceanogr 46: 765–777CrossRefGoogle Scholar
  91. Palmqvist K (2000) Carbon economy in lichens. New Phytol 148: 11–36CrossRefGoogle Scholar
  92. Palmqvist K, Samuelsson G and Badger MR (1994) Photobiontrelated differences in carbon acquisition among green algal lichens. Planta 195: 70–79.CrossRefGoogle Scholar
  93. Pearson GA, Serrao EA and Brawley SH (1998) Control of gamete release in fucoid algae: sensing hydrodynamic conditions via carbon acquisition. Ecology 79: 1725–1739CrossRefGoogle Scholar
  94. Poole LJ and Raven JA (1997) The Biology of Enteromorpha. Progr Phycol Res 12: 1–148Google Scholar
  95. 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, LondonGoogle Scholar
  96. Raven JA (1970) Exogenous inorganic carbon sources in plant photosynthesis. Biol Rev 45: 167–221Google Scholar
  97. 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.CrossRefGoogle Scholar
  98. Raven JA (1981) Nutritional strategies of submerged benthic plants: The acquisition of C, N and P by rhizophytes and haptophytes. New Phytol 88: 1–30CrossRefGoogle Scholar
  99. Raven JA (1982) The energetics of freshwater algae: Energy requirements for biosynthesis and volume regulation. New Phytol 92: 1–20CrossRefGoogle Scholar
  100. Raven JA (1984) Energetics and Transport in Aquatic Plants. A R Liss, New YorkGoogle Scholar
  101. 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 214Google Scholar
  102. Raven JA (1991) Implications of inorganic C utilization: Ecology, evolution and geochemistry. Can J Plant Physiol 69: 908–924Google Scholar
  103. 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: 477–485CrossRefGoogle Scholar
  104. Raven JA (1993b) Energy and nutrient acquisition by autotrophic symbioses and their asymbiotic ancestors. Symbiosis 14: 33–60Google Scholar
  105. Raven JA (1994) Why are there no picoplankton O2 evolvers with volumes less than 10¯19 m3? J Plankton Res 16: 565–580Google Scholar
  106. Raven JA (1995) Costs and benefits of low intracellular osmolarity in cells of freshwater algae. Funct Ecol 9: 701–707CrossRefGoogle Scholar
  107. Raven JA (1997a) Multiple origins of plasmodesmata. Eur J Phycol 32: 95–101CrossRefGoogle Scholar
  108. Raven JA (1997b) Phagotrophy in phototrophs. Limnol Oceanogr 42: 198–205Google Scholar
  109. Raven JA (1997c) Inorganic carbon acquisition by marine autotrophs. Adv Botan Res 27: 85–209Google Scholar
  110. Raven JA (1997d) Putting the C in phycology. Eur J Phycol 32: 319–333CrossRefGoogle Scholar
  111. Raven JA (1997e) The vacuole: A cost-benefit analysis. Adv Bot Res 25: 59–86CrossRefGoogle Scholar
  112. Raven JA (1998a) Small is beautiful. The picophytoplankton. Funct Ecol 12: 503–513CrossRefGoogle Scholar
  113. Raven JA (1998b) Picophytoplankton. Progr Phycol Res 13: 33–106Google Scholar
  114. Raven JA (1999a) The size of cells and organisms in relation to the evolution of embryophytes. Plant Biol 1: 2–12Google Scholar
  115. 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, LondonGoogle Scholar
  116. Raven JA (2003) Carboxysomes and peptidoglycan walls of cyanelles: possible physiological functions. Eur J Phycol 38: 47–53CrossRefGoogle Scholar
  117. Raven JA and Falkowski PG (1999) Oceanic sinks for atmospheric CO2. Plant Cell Environ 22: 741–755CrossRefGoogle Scholar
  118. Raven JA and Kübler JE (2002) New light on the scaling of metabolic rate with the size of algae. J Phycol 38: 11–16CrossRefGoogle Scholar
  119. 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: 41–47CrossRefGoogle Scholar
  120. 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: 407–417CrossRefGoogle Scholar
  121. 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: 537–545CrossRefGoogle Scholar
  122. 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: 355–378CrossRefGoogle Scholar
  123. 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: 525–536CrossRefPubMedGoogle Scholar
  124. 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: 409–422CrossRefGoogle Scholar
  125. 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: 937–944PubMedGoogle Scholar
  126. Rujin T and Martin W(2001) How many genes in Arabidopsis come from cyanobacteria? An estimate from 386 protein phylogenies. Trend Genet 17: 113–120CrossRefGoogle Scholar
  127. Sand-Jensen KAJ (1977) Effects of epiphytes on eelgrass photosynthesis. Aquat Bot 3: 55–63CrossRefGoogle Scholar
  128. Sand-Jensen K and Pedersen MF (1994) Photosynthesis by symbiotic algae in the freshwater sponge Spongilla lacustris. Limnol Oceanogr 39: 551–561Google Scholar
  129. Sand-Jensen K, Pedersen O and Geertz-Hansen O (1997) Regulation and role of photosynthesis in the colonial ciliate Ophrydium versatile. Limnol Oceanogr 42: 866–873Google Scholar
  130. Schaffelke B (1999) Particulate matter as an alternative nutrient source for tropical Sargassum species (Fucales, Phaeophyceae). J Phycol 33: 1150–1157CrossRefGoogle Scholar
  131. 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: 175–184CrossRefGoogle Scholar
  132. Serrao EA, Pearson G, Kauksky L and Brawley SH (1996) Successful external fertilization in turbulent conditions. Proc Natl Acad Sci USA 93: 3286–5290CrossRefGoogle Scholar
  133. Spalding MH, Van K, Wang Y and Nakamura Y (2002) Acclimation of Chlamydomonas to changing carbon availability. Funct Plant Biol 29: 221–230CrossRefGoogle Scholar
  134. 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: 730–739CrossRefGoogle Scholar
  135. 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: 969–974CrossRefGoogle Scholar
  136. 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: 3395–3421CrossRefGoogle Scholar
  137. 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: 113–125Google Scholar
  138. 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: 723–728CrossRefPubMedGoogle Scholar
  139. 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: 629–639CrossRefPubMedGoogle Scholar
  140. 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: 251–260CrossRefGoogle Scholar
  141. 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: 134–142CrossRefGoogle Scholar
  142. 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: 159–162CrossRefPubMedGoogle Scholar
  143. Tortell PD (2000) Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnol Oceanogr 45: 744–750CrossRefGoogle Scholar
  144. Tortell PD, Rau GH and Morel FMM (2000) Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnol Oceanogr 45: 1485–1500CrossRefGoogle Scholar
  145. 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: 185–195CrossRefGoogle Scholar
  146. Van den Hoek C, Mann DG and Jahns HM (1995) Algae. An Introduction to Phycology. Cambridge University Press, Cambridge, UKGoogle Scholar
  147. 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: 50–53CrossRefGoogle Scholar
  148. Williams SL (1984) Uptake of sediment ammonium and translocation in a marine macroalga Caulerpa cupressoides. Limnol Oceanogr 29: 374–379CrossRefGoogle Scholar
  149. Williams SL and Fisher TR (1985) Kinetics of nitrogen-15 labelled ammonium uptake by Caulerpa cupressoides (Chlorophyta). J Phycol 21: 287–296CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • John A. Raven
    • 1
  1. 1.Division of Environmental and Applied BiologySchool of Life Sciences, University of DundeeDundeeUK

Personalised recommendations