Skip to main content

Advertisement

SpringerLink
Log in

Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change

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

Abstract

Carbon dioxide concentrating mechanisms (also known as inorganic carbon concentrating mechanisms; both abbreviated as CCMs) presumably evolved under conditions of low CO2 availability. However, the timing of their origin is unclear since there are no sound estimates from molecular clocks, and even if there were, there are no proxies for the functioning of CCMs. Accordingly, we cannot use previous episodes of high CO2 (e.g. the Palaeocene–Eocene Thermal Maximum) to indicate how organisms with CCMs responded. Present and predicted environmental change in terms of increased CO2 and temperature are leading to increased CO2 and HCO3 − and decreased CO3 2− and pH in surface seawater, as well as decreasing the depth of the upper mixed layer and increasing the degree of isolation of this layer with respect to nutrient flux from deeper waters. The outcome of these forcing factors is to increase the availability of inorganic carbon, photosynthetic active radiation (PAR) and ultraviolet B radiation (UVB) to aquatic photolithotrophs and to decrease the supply of the nutrients (combined) nitrogen and phosphorus and of any non-aeolian iron. The influence of these variations on CCM expression has been examined to varying degrees as acclimation by extant organisms. Increased PAR increases CCM expression in terms of CO2 affinity, whilst increased UVB has a range of effects in the organisms examined; little relevant information is available on increased temperature. Decreased combined nitrogen supply generally increases CO2 affinity, decreased iron availability increases CO2 affinity, and decreased phosphorus supply has varying effects on the organisms examined. There are few data sets showing interactions amongst the observed changes, and even less information on genetic (adaptation) changes in response to the forcing factors. In freshwaters, changes in phytoplankton species composition may alter with environmental change with consequences for frequency of species with or without CCMs. The information available permits less predictive power as to the effect of the forcing factors on CCM expression than for their overall effects on growth. CCMs are currently not part of models as to how global environmental change has altered, and is likely to further alter, algal and aquatic plant primary productivity.

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

Abbreviations

CCM CO2 :

Concentrating mechanism

DOC:

Dissolved organic carbon

PAR:

Photosynthetically active radiation (400–700 nm)

Rubisco:

Ribulose bisphosphate carboxylase-oxygenase

UVA:

Ultraviolet A radiation (320–400 nm)

UVB:

Ultraviolet B radiation (280–320 nm)

References

  • Archer DE, Johnson K (2000) A model of the iron cycle in the ocean. Global Biogeochem Cycles 14:269–279

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Badger MR, Kaplan A, Berry JA (1980) Internal inorganic carbon pool of Chlmaydomonas reinhardtii. Plant Physiol 66:407–413

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Badger MR, Price GD, Long BM, Woodger FJ (2006) The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. J Exp Bot 57:249–265

    PubMed  CAS  Google Scholar 

  • Barschnagel RA (1966) New fossil algae from Middle Devonian of New York. Trans Am Microscop Soc 85:297–302

    Google Scholar 

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

    Google Scholar 

  • Beardall J, Giordano M (2002) Ecological implications of algal CCMs and their regulation (review). Funct Plant Biol 29:335–347

    CAS  Google Scholar 

  • Beardall J, Roberts S (1999) Inorganic carbon acquisition by two Antarctic macroalgae, Porphyra endivifolia (Rhodophyta: Bangiales) and Palmaria decipiens (Rhodophyta: Palmariales). Polar Biol 21:310–315

    Google Scholar 

  • Beardall J, Beer S, Raven JA (1998) Biodiversity of marine plants in an era of climate change. Some predictions based on physiological performance. Bot Mar 66:407–413

    Google Scholar 

  • Beardall J, Heraud P, Roberts S, Shelly K, Stojkovic S (2002) Effects of UV-B radiation in on inorganic carbon acquisition by the marine microalgae Dunaliella tertiolecta (Chlorophyceae). Phycologia 41:268–272.

    Google Scholar 

  • Beardall J, Roberts S, Raven JA (2005) Regulation of inorganic carbon acquisition by phosphorus limitation in the green alga Chlorella emersonii. Can J Bot 83:859–864

    CAS  Google Scholar 

  • Beardall J, Sobrino S, Stojkovic S (2009a) Interactions between impacts of ultraviolet radiation, elevated CO2, and nutrient limitation in marine primary producers. Photochem Photobiol Sci 8:1257–1265

    PubMed  CAS  Google Scholar 

  • Beardall J, Allen D, Bragg J, Finkel ZV, Flynn KV, Quigg A, Rees TAV, Richardson A, Raven JA (2009b) Allometry and stoichiometry of unicellular, colonial and multicellular phytoplankton. New Phytol 181:295–309

    PubMed  CAS  Google Scholar 

  • Beardall J, Stojkovic S, Larson S (2009c) Living in a high CO2 world; impacts of global climate change on marine phytoplankton. Plant Ecol Divers 2:191–205

    Google Scholar 

  • Behrenfeld MJ, O’Malley RT, Siegel DA, McClain CR, Sarmiento JL, Felman GC, Milligan AJ, Falkowski PG, Letelier RH, Bass EH (2006) Climate-driven trends in contemporary ocean productivity. Nature 444:752–755

    PubMed  CAS  Google Scholar 

  • Bell G, Collins S (2008) Experimental evolution and global change. Evol Appl 1:3–16

    Google Scholar 

  • Beman AM, Chow CE, King ALK, Fend Y, Fuhrmasn JA, Bates NR, Popp BN, Hutchins DA (2011) Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc Natnl Acad Scvi USA 108:208–213

    Google Scholar 

  • Berger SA, Diehl S, Stibor H, Trommer G, Ruhenstroth M (2010) Water temperature and stratification depth independently shift cardinal events during plankton spring succession. Global Change Biol 16:1954–1965

    Google Scholar 

  • Bopp L, Boucher O, Aumont O, Belviso S, Dufresne J-L, Pham M, Monfray P (2004) Will dimethylsulphide emissions amplify or alleviate global warming? A model study. Can J Fish Aquat Sci 61:826–835

    CAS  Google Scholar 

  • Bopp L, Aumont O, Cadule P, Alvain S, Gehlen M (2005) Response of diatom distribution to global warming and potential implications: a global model study. Geophys Res Lett 32:L19606

    Google Scholar 

  • Boyce DG, Lewis MR, Worm B (2010) Global phytoplankton decline over the past century. Nature 466:591–596

    PubMed  CAS  Google Scholar 

  • Boyd PW (2007) Biogeochemistry: iron findings. Nature 446:989–991

    PubMed  CAS  Google Scholar 

  • Boyd PW, Ibisanwi E, Sander SG, Hunter KA, Jackson GA (2010a) Remineralisation of upper ocean particles: Implications for iron biogeochemistry. Limnol Oceanogr 55:1271–1288

    CAS  Google Scholar 

  • Boyd PW, Strzepek R, Fu FX, Hutchins DA (2010b) Environmental control on open-ocean phytoplankton groups: now and in the future. Limnol Oceanogr 53:1353–1376

    Google Scholar 

  • Breitbarth E, Bellerby RJ, Neill CC, Ardelan MV, Meyerhofer M, Zollner E, Croot PL, Riebesell U (2010) Ocean acidification affects iron speciation during a coastal seawater mesocosm experiment. Biogeosci 7:1063–1073

    Google Scholar 

  • Burey SC, Poroyko V, Ergen ZN, Schuller C, Ohnishi N, Fukuzawa H, Bohnert HJ, Löffelhardt W (2007) Acclimation to low [CO2] by an inorganic carbon-concentrating mechanism in Cyanophora paradoxa. Plant Cell Environm 30:1422–1435

    CAS  Google Scholar 

  • Callieri C, Morobito G, Huot Y, Neale PJ, Litchman E (2001) Photosynthetic responses of pico- and nanoplanktonic algae to UVB, UVA, and PAR in a high mountain lake. Aquatic Sci 63:286–293

    Google Scholar 

  • Cerling TE, Quade J, Wang Y, Bowman JR (1989) Isotopes in soils and palaeosols as ecology and palaeontology indicators. Nature 341:138–139

    CAS  Google Scholar 

  • Cerling TE, Ehleringer JR, Harris JM (1998) Carbon dioxide starvation, the development of C-4 ecosystems, and mammalian evolution. Phil Trans R Soc Lond B 353:159–170

    CAS  Google Scholar 

  • Chen YLL, Chen HY, Jan S, Tuo SH (2009) Phytoplankton productivity enhancement and assemblage change in the upstream Kuroshio after typhoons. Mar Ecol Progr Ser 385:111–126

    CAS  Google Scholar 

  • Collins S (2011) Competition limits adaptation and productivity in a photosynthetic alga at elevated CO2. Proc Roy Soc B 278:247–255

    Google Scholar 

  • Collins S, Bell G (2004) Phenotypic consequences of 1000 generations of selection at elevated CO2 in a green alga. Nature 431:566–569

    PubMed  CAS  Google Scholar 

  • Collins S, Bell G (2006) Evolution of natural algal populations at elevated CO2. Ecol Lett 9:129–135

    PubMed  Google Scholar 

  • Collins S, Gardner A (2009) Integrating physiological, ecological and evolutionary timescales: a Price equation approach. Ecol Lett 12:744–757

    PubMed  Google Scholar 

  • Collins S, Sültemeyer D, Bell G (2006a) Rewinding the tape: selection of algae adapted to high CO2 at current and Pleistocene levels of CO2. Evoln 60:1392–1401

    CAS  Google Scholar 

  • Collins S, Sültemeyer D, Bell G (2006b) Changes in carbon uptake in populations of Chlamydomonas reinhardtii selected at high CO2. Plant Cell Environm 29:1812–1819

    CAS  Google Scholar 

  • Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323:1015–1015

    Google Scholar 

  • Cuvelier ML, Allen AE, Maren A, McCrow JP, Messié M, Tringe SG, Woyke T, Welsh RM, Ishoey T, Less J-H, Binder BJ, Dupont CL, Latasa M, Guigard C, Back KC, Dupont CL, Latasa M, Caleo E, Read B, Lasken RS, Chavez FP, Woprden AT (2010) Targetted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton. Proc Natnl Acad Sci USA 107:14679–14684

    CAS  Google Scholar 

  • De Stasio BT, Hill DK, Kleinhans JM, Nibbelink NP, Magnuson JJ (1996) Potential effects of global climate change on small north-temperature lakes: Physics, fish and plankton. Limnol Oceanogr 41:1136–1149

    Google Scholar 

  • Doney SC (2006) Plankton in a warmer world. Nature 444:605–696

    Google Scholar 

  • Doney SC, Lima L, Feely RA, Glover DM, Lindsay K, Mahowald N, Moore JK, Wanninkhof R (2009a) Mechanisms governing interannual variability in upper-ocean inorganic carbon system and air-sea CO2 fluxes. Deep-Sea Res II Topical Stud Oceanograph 56:640–655

    CAS  Google Scholar 

  • Doney SC, Fabry VJ, Feeley RA, Kleypas JA (2009b) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192

    Google Scholar 

  • Egge JK, Thingstad TF, Larsen A, Engel A, Wohlers J, Bellerby RGJ, Riebesell U (2009) Primary production during nutrient-induced blooms at elevated CO2 concentrations. Biogeosci 6:877–885

    CAS  Google Scholar 

  • Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, Princeton

    Google Scholar 

  • Feng Y, Warner ME, Zhang Y, Sun J, Fu FX, Rose JM, Hutchins DA (2008) Interactive effects of increased pCO2, temperature and irradiance on the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae). Eur J Phycol 43:87–98

    CAS  Google Scholar 

  • Feng Y, Hare CE, Leblanc K, Rose JM, Zhang Y, DiTullio GR, Lee PA, Wilhelm RW, Rowe JM, Sun J, Nemek M, Guegen C, Passow U, Benner I, Hutchins DA (2009a) The effects of increased pCO2 and temperature on the North Atlantic Spring Bloom. I. The phytoplankton community and biogeochemical responses. Mar Ecol Progr Ser 388:13–25

    CAS  Google Scholar 

  • Feng Y, Hare CE, Rose JM, Hardy SM, DiTullio GRS, Sun J, Lee PA, Smith WO, Peloquin J, Tozzi MC, Sohst B, Sun J, Zhang Y, Dunbar KB, Long MC, Sohst B, Hutchins DA (2009b) Interactive effects of iron, irradiance and CO2 on Ross Sea phytoplankton. Deep Sea Res 57:604–620

    Google Scholar 

  • Finkel ZV, Katz ME, Wright JD, Schofield OME, Falkowski PG (2005) Climatically driven patterns in the size of diatoms over the Cenozoic. Proc Natnl Acad Sci USA 102:8927–8932

    CAS  Google Scholar 

  • Finkel ZV, Beardall J, Flynn KJ, Quigg A, Rees TAV, Raven JA (2010) Phytoplankton in a changing world: cell size and elemental stoichiometry. J Plankt Res 32:119–137

    CAS  Google Scholar 

  • Fu XA, Han BP (2010) Response of cyanobacterial carbon concentrating mechanism to light intensity: a simulated analysis. Chinese J Oceanol Limnol 28:478–488

    CAS  Google Scholar 

  • Fu FX, Warren ME, Zhang YH, Feng YY, Hutchins DA (2007) Effects of increased temperature and CO2 on photosynthesis, growth and elemental ratios in marine Synechococcus and Prochlorococcus. J Phycol 43:485–496

    Google Scholar 

  • Fu FX, Zhang YH, Warner ME, Feng YY, Sun J, Hutchins DA (2008) A comparison of future increased CO2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum mimimum. Harmful Algae 7:76–90

    CAS  Google Scholar 

  • Gadd GM, Raven JA (2010) Geomicrobiology of eukaryotic microorganisms. Geomicrobiol J 27:491–519

    CAS  Google Scholar 

  • Galbraith ED, Gnanadedikan A, Dunne JP, Hiscock MR (2010) Regional impacts of iron-light colimitation in a global biogeochemical model. Biogeoscience 7:1043–1064

    CAS  Google Scholar 

  • Gao KS, Wu Y, Li G, Wu H, Villafañe VE, Helbling EW (2007) Solar UV radiation drives CO2 fixation in marine phytoplankton: a double-edged sword. Plant Physiol 144:54–59

    PubMed  CAS  Google Scholar 

  • Gao KS, Ruan ZX, Villafane VE, Gattuso JP, Helbling EW (2009) Ocean acidification exacerbates the effect of UV radiation on the calcifying phytoplankton Emiliana huxleyi. Limnol Oceanogr 54:1855–1862

    CAS  Google Scholar 

  • Ghannoum O, Conroy JP (2007) Phosphorus deficiency inhibits growth in parallel with photosynthesis in a C3 (Panicum laxum) but not two C4 (P. coloratum and Cenchrus ciliaris) grasses. Funct Plant Biol 34:72–81

    CAS  Google Scholar 

  • Ghannoum O, Paul MJ, Ward JL, Beale MH, Corol D-I, Conroy JP (2008) The sensitivity of photosynthesis to phosphorus deficiency differs between C3 and C4 grasses. Funct Plant Biol 25:213–221

    Google Scholar 

  • Giordano M (2001) Interactions between C and N metabolism in Dunaliella salina cells cultured at elevated CO2 and high N concentrations. J Plant Physiol 158:577–581

    CAS  Google Scholar 

  • Giordano M, Bowes G (1997) Gas exchanges, metabolism, and morphology of Dunaliella salina in response to the CO2 concentration and nitrogen source used for growth. Plant Physiol 115:1049–1056

    PubMed  CAS  Google Scholar 

  • Giordano M, Norici A, Forssen M, Eriksson M, Raven JA (2003) An anaplerotic role for mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 132:2126–2134

    PubMed  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

    PubMed  CAS  Google Scholar 

  • Giráldez N, Aparicio PJ, Quiñones MA (1998) Blue light requirements for HCO3 − uptake and its action spectrum in Monoraphidium braunii. Photochem Photobiol 68:420–426

    Google Scholar 

  • Gnanadesikan A, Vecchi GA, Anderson WG, Hallberg R, Emanuel K (2010) How ocean color can steer Pacific tropical cyclones. Geophys Res Lett 37:L18802

    Google Scholar 

  • Gruber N, Gloor M, Fletcher SEM, Doney SC, Dutkeiwicz S, Follows S, Gerber MJ, Jacobson AR, Joos F, Lindsay K, Meneenlis D, Mouchet A, Muller SA, Sarmieinto JL, Takahashi T (2009) Ocean sources, sinks and transport of CO2. Global Biogeochem Cycles 23: Art No. GB 10052009

  • Halldall P (1964) Ultraviolet action spectra of photosynthesis and photosynthetic inhibition in a green and red alga. Physiol Plant 17:414–424

    Google Scholar 

  • Halldall P (1967) Ultraviolet action spectra in algology. A review. Photochem Photobiol 6:445–460

    Google Scholar 

  • Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rawley SJ, Tedesco D, Buia M-C (2008) Volcanic carbon dioxide vents reveal ecosystem effects of ocean acidification. Nature 454:96–99

    PubMed  CAS  Google Scholar 

  • Henderson SA, von Caemmerer S, Farquhar GD (1992) Short term measurements of carbon isotope discrimination in several C4 species. Austr J Plant Physiol 19:263–285

    CAS  Google Scholar 

  • Henson SA, Sarmineto JL, Dunne JP, Bopp L, Lima I, Doney SC, Beaulieu C (2010) Detection of anthropogenic climate change in satellite records of ocean chlorophyll and productivity. Biogeosci 7:621–649

    CAS  Google Scholar 

  • Herfort L, Loste E, Meldrum F, Thake B (2004) Structural and physiological effects of calcium and magnesium in Emiliania huxleyi (Lohman) Hay and Mohler. J Struct Biol 148:307–314

    PubMed  CAS  Google Scholar 

  • Hu HH, Gao KS (2008) Impacts of CO2 enrichment on growth and photosynthesis in freshwater and marine diatoms. Chinese J Oceanol Limnol 26:407–414

    CAS  Google Scholar 

  • Hu HH, Zhou QB (2010) Regulation of inorganic carbon acquisition by nitrogen and phosphorus levels in the Nannnochloropsis sp. World J Microbiol Biotech 26:957–961

    CAS  Google Scholar 

  • Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA (2009) Testing the effects of ocean acidification on algal metabolism: considerations for experimental design. J Phycol 45:1030–1051

    Google Scholar 

  • Hutchins DA, Hare CE, Weaver RS, Zhang Y, Firme GF, DiTullio GR, Alm MB, Risemanr SF, Mauchner JM, Geesey ME, Trick CG, Smith GJ, Rue EL, Conn J, Bruland KW (2002) Phytoplankton limitation in the Humboldt Current and Peru upwelling. Limnol Oceanogr 47:997–1011

    Google Scholar 

  • Iglesias-Rodríguez MD, Nimer NA, Merrett MJ (1998) Carbon dioxide-concentrating mechanism and the development of extracellular carbonic anhydrase in the marine picoeukaryote Micromonas pusilla. New Phytol 140:685–690

    Google Scholar 

  • Iglesias-Rodriguez MD, Halloran PR, Rickaby REM, Hall IR, Colmenero-Hidalgo E, Gittins JR, Green DRM, Tyrrell T, Gibbs SJ, von Passow P, Rehm E, Armbrust EV, Boessenkoot KP (2008) Phytoplankton calcification in a high-CO2 world. Science 320:336–340

    PubMed  CAS  Google Scholar 

  • Im CS, Zhnag Z, Shrager J, Chang CW, Grossman AR (2003) Analysis of light and CO2 regulation in Chlamydomonas reinhardtii using genome-wide approaches. Photosynth Res 75:111–125

    PubMed  CAS  Google Scholar 

  • Jardiller L, Zubkov MV, Pearman J, Scanlan DJ (2010) Significant CO2 fixation by small Prymnesiophyceae in the subtropical and tropical Northeast Atlantic Ocean. ISME J 4:1180–1192

    Google Scholar 

  • Johnston AM, Raven JA (1986) The analysis of photosynthesis in air and water by Ascophyllum nodosum (L) Le Jol. Oecologia 69:288–295

    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 

  • Joint I, Doney SC, Karl DM (2010) Will ocean acidification affect marine microbes. ISME J 5:1–7

    Google Scholar 

  • Kaplan A, Badger MR, Berry JA (1980) Photosynthesis and the intracellular inorganic carbon pool in the blue green alga Anabaena variabilis: response to external CO2 concentration. Planta 149:219–226

    CAS  Google Scholar 

  • Karlsson J, Byström P, Ask J, Ask P, Persson L, Jansson M (2009) Light limitation of nutrient-poor lake ecosystems. Nature 460:506–509

    PubMed  CAS  Google Scholar 

  • Key T, McCarthy A, Campbell DA, Six C, Roy S, Finkel ZV (2010) Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environ Microbiol 12:95–104

    PubMed  CAS  Google Scholar 

  • Klavsen SK, Maberly SC (2010) Effect of light and CO2 on inorganic carbon uptake in the invasive aquatic CAM-plant Crassula helmsii. Funct Plant Biol 37:737–747

    CAS  Google Scholar 

  • Knutson TR, McBride JL, Chan J, Emanuel K, Holland G, Landsea C, Held I, Kossin JP, Srivastave AK, Sugi M (2009) Tropical cyclones and climate change. Nat Geosci 3:157–163

    Google Scholar 

  • Korb RE, Raven JA, Johnston AM, Leftley JW (1996) Effect of cell size and specific growth rate on stable carbon isotope discrimination by two species of marine diatom. Mar Ecol Progr Ser 143:283–288

    Google Scholar 

  • Korb RE, Raven JA, Johnston AM (1998) Relationship between aqueous CO2 concentrations and stable carbon isotope discrimination in the diatoms Chaetoceros calcitrans and Ditylum brightwellii. Mar Ecol Progr Ser 171:303–305

    CAS  Google Scholar 

  • Kozłowska-Szerernos B, Bialuk I, Maleszewski S (2004) Enhancement of photosynthetic O2 evolution in Chlorella vulgaris under high light and increased CO2 concentration as a sign of acclimation to phosphate deficiency. Plant Physiol Biochem 42:403–409

    Google Scholar 

  • Kranz SA, Levitan O, Richter K-U, Prášil O, Berman-Frank O, Rost B (2010) Combined effects of CO2 and light on the N2 fixing cyanobacterium Trichodesmium IMS101: Physiological responses. Plant Physiol 154:334–345

    PubMed  CAS  Google Scholar 

  • Landry MR, Brown SL, Rii YM, Selph KE, Bidigare RR, Yang EJ, Simmons MR (2008) Depth-stratified phytoplankton dynamics in Cyclone Opal, a subtropical mesoscale eddy. Deep-Sea Res II 55:1348–1359

    Google Scholar 

  • Laws EA, Popp BN, Cassar N, Tanimoto J (2002) 13C discrimination patterns in oceanic phytoplankton: likely influence of CO2 concentrating mechanisms, and implications for palaeoreconstructions. Funct Plant Biol 29:323–333

    CAS  Google Scholar 

  • Lenton A, Codron F, Bopp L, Metzl N, Cadule P, Tagliabue A, Le Sommer J et al (2009) Stratospheric ozone depletion reduces ocean carbon uptake and enhances ocean acidification. Geophys Res Lett 36:L12606

    Google Scholar 

  • Leonardos N, Geider RJ (2009) No mechanistic dependence of photosynthesis on calcification in Emiliania huxleyi (Haptophyta). J Phycol 45:1046–1051

    Google Scholar 

  • Levitan O, Kranz SA, Spungin D, Prášil O, Rost B, Berman-Frank O (2010) Combined effects of CO2 and light on the N2 fixing cyanobacterium Trichodesmium IMS101: A mechanistic view. Plant Physiol 154:346–356

    PubMed  CAS  Google Scholar 

  • Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Annu Rev Ecol Evol Syst 39:615–639

    Google Scholar 

  • Liu H, Probert I, Uitz J, Claustre H, Aris-Broseau S, Froda M, Not F, de Vargas C (2009) Haptophytes rule the waves: extreme oceanic biodiversity in non-calcifying prymnesiophytes explains the 19-Hex paradox. Proc Natnl Acad Sci USA 106:12803–12808

    CAS  Google Scholar 

  • Maberly SC (1985) Photosynthesis by Fontinalis antipyretica. I. Interaction between photon irradiance, concentration of carbon and temperature. New Phytol 100:127–140

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

    CAS  Google Scholar 

  • Maberly SC, Madsen TV (1990) Contribution of air and water to the carbon balance of Fucus spiralis. Mar Ecol Progr Ser 62:175–183

    Google Scholar 

  • Maberly SC, Ball LA, Raven JA, Sültemeyer D (2009) Inorganic carbon acquisition by chrysophytes. J Phycol 45:1052–1061

    CAS  Google Scholar 

  • Madsen TV (1987) The effect of different growth conditions on dark and light carbon assimilation in Littorella uniflora. Physiol Plant 70:183–188

    CAS  Google Scholar 

  • Marbà N, Duarte CM, Agusti S (2007) Allometric scaling of plant life history. Proc Nat Acad Sci USA 104:1577–15780

    Google Scholar 

  • McLeod GC, Kanwisher J (1962) The quantum efficiency of photosynthesis in the ultraviolet light. Physiol Plant 15:581–586

    CAS  Google Scholar 

  • Mengelt C, Prézelin BB (2005) UVA enhancement of carbon fixation and resilience to UV inhibition in the genus Pseudo-Nitzschia may provide a competitive advantage in high UV surface waters. Mar Ecol Progr Ser 301:81–93

    CAS  Google Scholar 

  • Meyer M, Seibt U, Griffiths H (2008) To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms. Phil Trans R Soc Lond B 363:2767–2778

    CAS  Google Scholar 

  • Middelboe AL, Hansen PJ (2007) High pH in shallow-water macroalgal habitats. Mar Ecol Progr Ser 338:107–117

    CAS  Google Scholar 

  • Milligan AJ, Varela DE, Brzezinski MA, Morel FMM (2004) Dynamics of silicon metabolism and silicon isotope discrimination in a marine diatom as a function of pCO2. Limnol Oceanogr 49:322–329

    CAS  Google Scholar 

  • Mitchell C, Beardall J (1996) Inorganic carbon uptake by the sea ice diatom Nitzschia frigida. Polar Biol 16:95–99

    Google Scholar 

  • Monteith DT, Stoddard JL, Evans CD, de Wit HA, Forsius M, Høgåsen T, Wilander A, Skjelvåle LB, Jefferies DS, Vuovenman J, Keller B, Kopácek J, Vesely J et al (2007) Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450:537–540

    PubMed  CAS  Google Scholar 

  • Muller MN, Schulz KG, Riebesell U (2010) Effects of long-term high CO2 exposure on two species of coccolithophore. Biogeoscience 7:1109–1116

    Google Scholar 

  • Not F, Latasa M, Marie D, Cariou T, Vaulot D, Simon N (2004) A single species, Micromonas pusilla (Prasinophyceae), dominates the eukaryotic picoplankton in the Western English Channel. Appl. Env Microbiol 70:4064–4072

    CAS  Google Scholar 

  • Oehler DZ (1976) Transmission electron microscopy of organic microfossils from late Precambrian Bitter Springs formation in Australia: techniques and survey of preserved ultrastructure. J Palaeontol 50:90–106

    Google Scholar 

  • Oehler DZ (1977) Pyrenoid-like structures in the Precambrian algae from the Bitter Springs formation of Australia. J Palaeontol 51:885–901

    Google Scholar 

  • Osborne CP, Beerling DJ (2006) Nature’s green revolution: the remarkable evolutionary rise of C4 plants. Phil Trans R Soc B 361:173–194

    PubMed  Google Scholar 

  • Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58

    PubMed  CAS  Google Scholar 

  • Palenik B, Grimwood J, Aerts A, Razé P, Salamov A, Putnam N, Dupont C, Jorgensen R, Denelle E, Rombauts S, Zho K, Otillar R, Mechant SS, Padell S, Gasterland T, Napoli C, Gentler K, Manuell A, Tai V, Vallon O, Pignaneau G, Joncek S, Heijde M, Dubchek T, Pazour S, Werner G, Dubchak I, Pazour GJ, can de Peer Y, Moreau M, Grigoriev IV (2007) The tiny eukaryote Ostreococcus provides genomic insight into the paradox of the plankton. Proc Natnl Acad Sci USA 104:7705–7710

    CAS  Google Scholar 

  • Palinska KA, Laloui W, Bédu S, Loiseaux-de Goër S, Catsets AM, Rippka R, Tandeau de Marsac N (2002) The signal transducer PII and bicarbnonate acquisition in Prochlorococcus marinus PCC 9511, a marine cyanobacterium naturally deficient in nitrate and nitrite assimilation. Microbiology 148:2405–2412

    PubMed  CAS  Google Scholar 

  • Palmqvist K (1993) Photosynthetic CO2-use efficiency in lichens and their isolated photobionts. Planta 191:48–56

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Palmqvist K, de los Rios A, Ascaso C, Samuelsson G (1997) Photosynthetic carbon acquisition in the lichen photobionts Coccomyxa and Trebouxia (Chlorophyta). Physiol Plant 101:67–76

    CAS  Google Scholar 

  • Parekh P, Follows MJ, Boyle EA (2004) Modelling the global ocean iron cycle. Global Biogeochem Cycles 18:GB1002

    Google Scholar 

  • Pengelty JPL, Sirault XRR, Tazoe Y, Evans JR, Furbank RT, von Caemmerer S (2010) Growth of the C4 dicot Flaveria bidentis: photosynthetic acclimation to low light through shifts in leaf anatomy and biochemistry. J Exp Bot 61:4109–4122

    Google Scholar 

  • Poorter H, Gifford RM, Kriedemann PE, SCl Wong (1992) A quantitative analysis of dark respiration and carbon content as factors in the growth-response of plants to elevated CO2. Austr J Bot 40:501–513

    CAS  Google Scholar 

  • Price GD, Badger MR, Woodger FI, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59:1441–1461

    PubMed  CAS  Google Scholar 

  • Ratti S, Giordano M, Morese F (2007) CO2-concentrating mechanism of the potentially toxic dinoflagellate Protoceratium reticulatum (Dinophyceae, Gonyaulacales). J Phycol 53:393–401

    Google Scholar 

  • Raven JA (1990) Predictions of Fe and Mn use efficiencies of phototrophic growth as a function of light availability for growth and C assimilation pathway. New Phytol 116:1–18

    CAS  Google Scholar 

  • Raven JA (1991a) Implications of inorganic carbon utilization—ecology, evolution and geochemistry. Can J Bot 69:908–924

    CAS  Google Scholar 

  • Raven JA (1991b) Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: relation to increased CO2 and temperature. Plant Cell Environ 14:779–794

    CAS  Google Scholar 

  • Raven JA (1997) The role of marine biota in the evolution of terrestrial biota: gases and genes–atmospheric composition and evolution of terrestrial biota. Biogeochem 39:139–164

    Google Scholar 

  • Raven JA (2010) Inorganic carbon acquisition by eukaryotic algae: four current questions. Photosynth Res 106:123–134

    Google Scholar 

  • Raven JA (2011) Carbon. In: Whitton B (ed) Ecology of cyanobacteria, 2nd edn. Springer, Berlin (in press)

    Google Scholar 

  • Raven JA, Andrews M (2010) Evolution of tree nutrition. Tree Physiol 30:1050–1071

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Raven JA, Geider RJ (1988) Temperature and algal growth. New Phytol 110:441–461

    CAS  Google Scholar 

  • Raven JA, Geider RD (2003) Adaptation, acclimation and regulation of photosynthesis in algae. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer, Dordrecht, pp 385–412

    Google Scholar 

  • Raven JA, Johnston AM (1991) Mechanisms of inorganic carbon acquisition in marine phytoplankton, and their implications for the use of other resources. Limnol Oceanogr 36:1701–1714

    CAS  Google Scholar 

  • Raven JA, Waite A (2004) Tansley review: the evolution of silicification in diatoms: inescapable sinking and sinking as escape? New Phyt 162:45–61

    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 (2002a) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378

    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, Fredriksen S, Dunton KH (2002b) Seaweeds in cold seas: evolution and carbon acquisition. Ann Bot 90:525–536

    PubMed  CAS  Google Scholar 

  • Raven JA, Ball LA, Beardall J, Giordano M, Maberly SC (2005a) Algae lacking carbon concentrating mechanisms. Can J Bot 83:879–890

    CAS  Google Scholar 

  • Raven JA, Brown K, Mackay M, Beardall J, Giordano M, Granum E, Leegood RC, Kilminster K, Walker DI (2005b) Iron, nitrogen, phosphorus and zinc cycling and consequences for primary productivity in the oceans. In: Gadd GM, Semple KT, Lappin-Scott HM (eds) Society for general microbiology symposium 65 micro-organisms and earth systems: advances in geobiology. Cambridge University Press, Cambridge, pp 247–272

  • Raven JA, Cockell CS, La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Phil Trans Roy Soc B 363:2641–2650

    CAS  Google Scholar 

  • Reinfelder JR (2011) Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu Rev Mar Sci 3:291–315

    Google Scholar 

  • Renberg L, Johansson AI, Shutova S, Stenlund H, Aksman A, Raven JA, Gardeström P, Moritz T, Samuelssson G (2010) A metabolomic approach to study major metabolite changes during acclimation to limiting CO2 in Chlamydomonas reinhardtii. Plant Physiol 154:187–196

    PubMed  CAS  Google Scholar 

  • Richardson AJ (2008) In hot water: zooplankton and climate change. ICES J Mar Sci 65:279–295

    Google Scholar 

  • Riding R (2006) Cyanobacterial calcification, carbon dioxide concentrating mechanisms and Proterozoic-Cambrian changes in atmospheric composition. Geobiology 4:299–316

    CAS  Google Scholar 

  • Riding R (2009) An atmospheric stimulus for cyanobacterial-induced calcification ca. 350 million years ago? Palaios 24:685–696

    Google Scholar 

  • Riebesell U (2004) Effects of CO2 enrichment on marine phytoplankton. J Oceanogr 60:719–729

    CAS  Google Scholar 

  • Riebesell U, Schulz KG, Bellerby RGJ, Botros M, Fritsche P, Meyerhöfer M, Neill C, Nondol G, Oschlies A, Wohlers J, Zöllner E (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450:545–548

    PubMed  CAS  Google Scholar 

  • Riebesell U, Kortzinger A, Oschlies A (2009) Sensitivities of marine carbon fluxes to ocean change. Proc Natnl Acad Sci USA 106:20602–20609

    CAS  Google Scholar 

  • Riebesell U, Fabry VJ, Nansson LN, Gattuso J-P (eds) (2010) Guide to best practices for ocean acidification research and data reporting. 260 pp. Luxembourg: Publications Office of the European Union. http://www.epoca-project.eu/index.php/guide-to-best-practices-for-ocean-acidification-research-and-data-reporting.htm

  • Robarts RD, Waiser MJ, Hadas O, Zophary T, MacIntyre S (1998) Relaxation of phosphorus limitation due to typhoon-induced mixing in two morphologically distinct basins of Lake Biwa, Japan. Limnol Oceanogr 43:1023–1036

    CAS  Google Scholar 

  • Rost B, Zondervan I, Wolf-Gladrow D (2008) Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions. Mar Ecol Progr Ser 373:227–237

    CAS  Google Scholar 

  • Schulz KG, Ramos JBE, Zeebe RE, Riebesell U (2009) CO2 perturbation experiments: similarities and differences between dissolved inorganic carbon and total alkalinity manipulations. Biogeoscience 6:2145–2153

    CAS  Google Scholar 

  • Shapiro J (1997) The role of carbon dioxide in the initiation and maintenance of blue-green dominance in lakes. Freshwat Biol 37:307–323

    Google Scholar 

  • Shi D, Xu Y, Morel FMM (2009) Effects of the pH/pCO2 control method on medium chemistry and phytoplankton growth. Biogeoscience 6:1199–1207

    CAS  Google Scholar 

  • Shi D, Hopkinson BM, Morel FMM (2010) Effect of ocean acidification in iron availability to marine phytoplankton. Science 327:676–679

    PubMed  CAS  Google Scholar 

  • Smith EC, Griffiths H (1996) The occurrence of the chloroplast pyrenoid is correlated with the activity of a CO2-concentrating mechanism and carbon isotope discrimination in lichens and bryophytes. Planta 198:6–16

    CAS  Google Scholar 

  • Sobrino C, Ward ML, Neale PJ (2008) Acclimation of elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnol Oceanogr 53:494–505.

    CAS  Google Scholar 

  • Sobrino C, Neale PJ, Phillips-Kress JD, Moeller RE, Porter JA (2009) Elevated CO2 increases sensitivity to ultraviolet radiation in lacustrine phytoplankton assemblages. Limnol Oceanogr 54:2448–2459

    CAS  Google Scholar 

  • Song YF, Qiu BS (2007) The CO2 concentrating mechanism in the bloom-forming cyanobacterium Microcystis aeruginosa (Cyanophyceae) and effects of UVB radiation on its operation. J Phycol 43:957–964

    CAS  Google Scholar 

  • Steinacher M, Joos F, Frolicher TL, Bopp L, Cadule P, Cocco V, Doney SC, Gehlen M, Lindsay K, Moore JK, Schneider B, Segschneider J (2010) Projected 21st century decrease in marine primary productivity: a multi-model analysis. Biogeosci 7:979–1005

    CAS  Google Scholar 

  • Surif MB, Raven JA (1990) Photosynthetic gas exchange under emersed conditions in eulittoral and normally submersed members of the Fucales and the Laminariales: Interpretation in relation to C isotope ratio and N and water use efficiency. Oecologia 82:68–80

    Google Scholar 

  • Tazoe Y, Hanba YT, Furumoto T, Noguchi K, Terashima I (2008) Relationships between quantum yield for CO2 assimilation activity of key enzymes and CO2 leakiness in Amaranthus cruentus, a C4 dicot, grown in high or low light. Plant Cell Physiol 49:19–29

    PubMed  CAS  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 Natnl Acad Sci USA 103:7246–7251

    CAS  Google Scholar 

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

    PubMed  CAS  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 environment. Phosynth Res 77:95–103

    CAS  Google Scholar 

  • The Royal Society (2005) Ocean acidification due to increased carbon dioxide. Policy Document 12/05. The Royal Society, London

    Google Scholar 

  • Theodorou ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphorus deprivation. Plant Physiol 101:339–344

    PubMed  CAS  Google Scholar 

  • Tortell PD, Payne CD, Li Y, Trimborn S, Rost B, Smith WO, Riesselman C, Dunbar RR, Sedwick P, DiTullio GR (2008a) CO2 sensitivity of Southern Ocean phytoplankton. Geophys Res Lett 35:L04605

    Google Scholar 

  • Tortell PD, Payne C, Guegon C, Strzepek RF, Boyd PW, Rost B (2008b) Inorganic carbon uptake by Southern Ocean phytoplankton. Limnol Oceanogr 53:1266–1278

    CAS  Google Scholar 

  • Tortell PD, Trimborn S, Li Y, Rost B, Payne CD (2010) Inorganic carbon utilization by Ross Sea phytoplankton across natural and experimental CO2 gradients. J Phycol 46:433–443

    CAS  Google Scholar 

  • Tranvik LJ, Downing JA, Cotner JB et al (2009) Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr 54:2298–2314

    CAS  Google Scholar 

  • Trimborn S, Langer G, Rost B (2007) Effect of varying calcium concentrations and light intensities on calcification and photosynthesis in Emiliania huxleyi. Limnol Oceanogr 52:2285–2293

    CAS  Google Scholar 

  • Uitz H, Claustre H, Gentoli B, Stramski D (2010) Phytoplankton class-specific primary production in the world’s oceans; seasonal and interannual variability from satellite observations. Glob Biogeochem Cycles 24(3):GB 2016

    Google Scholar 

  • van de Poll WHV, van Leeuwe MA, Roggeveld J, Buma AGJ (2005) Nutrient limitation and high irradiance acclimation reduce photosynthetically active radiation and UV-induced viability loss in the Antarctic diatom Chaetoceros brevis (Bacillariophyceae). J Phycol 41:840–850

    Google Scholar 

  • van de Poll WHV, Janknegt PJ, van Leeuwe MA, Visser RJW, Buma AGJ (2009) Excessive irradiance and antioxidant responses of an Antarctic marine diatom exposed to iron limitation and to dynamic irradiance. J Photochem Photobiol 94:32–37

    Google Scholar 

  • Vance P, Spalding MH (2005) Growth, photosynthesis, and gene expression in Chlamydomonas over a range of CO2 concentrations and CO2/O2 ratios: CO2 regulates multiple acclimation states. Can J Bot 83:796–809

    CAS  Google Scholar 

  • Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochem 57(58):1–45

    Google Scholar 

  • Weng XY, Xu HX, Yang Y, Peng HH (2008) Water-water cycle involved in dissipation of excess photon energy in phosphorus deficient rice leaves. Photosynthetica 52:307–313

    CAS  Google Scholar 

  • Wetz MS, Paerl HW (2008) Estuarine phytoplankton responses to hurricanes and tropical storms with different characteristics (trajectory, rainfall, winds). Estuaries Coasts 31:419–429

    CAS  Google Scholar 

  • Wienkoop S, Weiβ J, May R, Kempa S, Irgang S, Recuenco-Munoz L, Pietzke M, Schwemmer T, Rupprect J, Egenhofer V, Weckwerth W (2010) Targetted proteomics for Chlamydomonas reinhardtii combined with rapid subcellular protein fractionation, metabolomics and metabolic flux analysis. Mol BioSyst 6:1018–1031

    PubMed  CAS  Google Scholar 

  • Williamson CE, Sternberger RS, Morris DP, Frost TM, Paulsen SG (1996) Ultraviolet radiation in North American lakes: attenuation estimates from DOC measurements and implications for plankton communities. Limnol Oceanogr 41:1024–1034

    CAS  Google Scholar 

  • Winter K, Schmitt MR, Edwards GR (1982) Microstegium vimineum, a shade adapted C4 grass. Plant Sci Lett 24:311–318

    Google Scholar 

  • Worden AZ, Leee J-H, Mock T, Rouzé P, Simmons MP, Aerts AL, Allen AE, Cuvellier ML, Denelle E, Everett MV, Foulon E, Grimwood J, Groundlackh H, Henrissat S, Napoli C, McDonald SM, Parker MS, Romnbauts S, Salamov A, von Dassopw P, Badger JH, Couinho PH, Demir E, Dubchak I, Genteman C, Eikrem W, Gready JE, John U, Larrier W, Lundquist EA, Lucas S, Maxyer KFX, Moreau H, Not F, Otillar R, Panaud O, Pangillar J, Paulsen I, Piegu B, Paliakov A, RobbersS SchmitzJ, Toulza E, Wyss T, Zelensky A, Zhou K, van de Peer Y, Grigoriev IV (2009) Green evolution and dynamic adaptation revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268–272

    PubMed  CAS  Google Scholar 

  • Wu HY, Zou DH, Gao KS (2008) Impacts of increased atmospheric CO2 concentration on photosynthesis and growth of micro- and macro-algae. Sci in China C Life Sci 51:1144–1150

    Google Scholar 

  • Wu Y, Gao K, Riebesell U (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylyum tricornutum. Biogeosciences 7:2915–2923

    CAS  Google Scholar 

  • Xu ZG, Gao KS (2009) Impacts of UV radiation on growth and photosynthetic carbon acquisition in Gracilaria lemanaeiformis (Rhodophyta) under phosphorus-limited and replete conditions. Funct Plant Biol 36:1057–1064

    CAS  Google Scholar 

  • Xu J, Gao GK (2010) Use of UVA energy for photosynthesis in the red macroalga Gracilaria lemanaeiformis. J Photochem Photobiol 86:580–585

  • Young EB, Beardall J (2005) Modulation of photosynthesis and inorganic acquisition in a marine microalga by nitrogen, iron and light availability. Can J Bot 83:917–928

    CAS  Google Scholar 

  • Zeebe RE, Wolf-Gladrow D (2001) CO2 in seawater: equilibrium, kinetics, isotopes. Elsevier oceanography series, vol 65. Elsevier, Amsterdam, p xiii + 346

  • Zondervan I (2007) The effects of light, macronutrients, trace metals and CO2 on the production of calcium carbonate and organic carbon in coccolithophores—a review. Deep-Sea Res II 54:521–537

    Google Scholar 

Download references

Acknowledgments

Comments from two anonymous referees were very useful. The University of Dundee is a registered Scottish Charity, No SC010596. JAR’s research on inorganic carbon acquisition was funded by BBSRC UK and NERC UK. JB is grateful to the Australian Research Council for their support of his study on inorganic carbon acquisition in relation to climate change. MG’s research on CCMs was partially funded by the Fondazione Cariverona, Italy, Ministry for Agriculture and Forestry, Italy and by the Southeast Wisconsin Energy Technology Research Center, USA.

Author information

Authors and Affiliations

  1. Division of Plant Sciences, University of Dundee at SCRI, Scottish Crop Research Institute, Invergowrie, Dundee, DD2 5DA, UK

    John A. Raven

  2. Department of Marine Sciences, Universitá Politecnica delle Marche, 60131, Ancona, Italy

    Mario Giordano

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

    John Beardall

  4. Centre for Ecology and Hydrology, Lancaster Environment Centre, Library Avenue, Bailrigg, Lancaster, LA1 4AP, UK

    Stephen C. Maberly

Authors
  1. John A. Raven
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mario Giordano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John Beardall
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stephen C. Maberly
    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., Giordano, M., Beardall, J. et al. Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynth Res 109, 281–296 (2011). https://doi.org/10.1007/s11120-011-9632-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-011-9632-6

Keywords

Search

Navigation