Abstract
Diatoms are responsible for up to 40% of primary productivity in the ocean, and complete genome sequences are available for two species. However, there are very significant gaps in our understanding of how diatoms take up and assimilate inorganic C. Diatom plastids originate from secondary endosymbiosis with a red alga and their Form ID Rubisco (ribulose-1,5-bisphosphate carboxylase-oxygenase) from horizontal gene transfer, which means that embryophyte paradigms can only give general guidance as to their C acquisition mechanisms. Although diatom Rubiscos have relatively high CO2 affinity and CO2/O2 selectivity, the low diffusion coefficient for CO2 in water has the potential to restrict the rate of photosynthesis. Diatoms growing in their natural aquatic habitats operate inorganic C concentrating mechanisms (CCMs), which provide a steady-state CO2 concentration around Rubisco higher than that in the medium. How these CCMs work is still a matter of debate. However, it is known that both CO2 and HCO −3 are taken up, and an obvious but as yet unproven possibility is that active transport of these species across the plasmalemma and/or the four-membrane plastid envelope is the basis of the CCM. In one marine diatom there is evidence of C4-like biochemistry which could act as, or be part of, a CCM. Alternative mechanisms which have not been eliminated include the production of CO2 from HCO −3 at low pH maintained by a H+ pump, in a compartment close to that containing Rubisco.
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References
Allen AE, Vardi A, Bowler C (2006) An ecological and evolutionary context for integrating nitrogen metabolism and related signalling pathways in marine diatoms. Curr Opinion Plant Biol 9:264–273
Apt KE, Zaslavkaia L, Lippmeier JC et al (2002) In vivo characterization of diatom multipartite plastid targeting signals. J Cell Sci 115:4061–4069
Armbrust EV, Berges JA, Bowler C et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution and metabolism. Science 306:79–86
Badger MR, Andrews TJ, Whitney SM et al (1998) The diversity and co-evolution of Rubisco, plastids, pyrenoids and chloroplast-based CO2 concentrating mechanisms in algae. Can J Bot 76:1052–1071
Badger MR, Price GD, Long BM et al (2006) The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. J Exp Bot 57:249–265
Baldauf SL (2003) The deep roots of eukaryotes. Science 300:1703–1706
Banse K (1982) Cell volumes, maximal growth rates of unicellular algae and ciliates, and the role of ciliates in the marine pelagial. Limnol Oceanogr 27:1059–1071
Barker HA (1935) Photosynthesis in diatoms. Arch Mikrobiol 6:141–156
Beardall J, Mukerji D, Glover HE et al (1976) The path of carbon in photosynthesis by marine phytoplankton. J Phycol 12:409–417
Birmingham BC, Colman B (1979) Measurement of carbon dioxide compensation points in freshwater algae. Plant Physiol 64:892–895
Birmingham BC, Coleman JR, Colman B (1982) Measurement of photorespiration in algae. Plant Physiol 69:259–262
Boldt R, Edner C, Kolukisaoglu U et al (2005) D-GLYCERATE 3-KINASE, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family. Plant Cell 17:2413–2420
Boyd C, Gradmann D (1999) Electrophysiology of the marine diatom Coscinodiscus wailesii. I. Endogenous changes in the membrane voltage and resistance. J Exp Bot 50:445–452
Burkhardt S, Amoroso G, Riebesell U et al (2001) CO2 and HCO −3 uptake in marine diatoms acclimated to different CO2 concentrations. Limnol Oceanogr 46:1378–1391
Burns BD, Beardall J (1987) Utilization of inorganic carbon by marine microalgae. J Exp Mar Biol Ecol 107:75–86
Cassar N, Laws EA, Popp BN et al (2002) Sources of inorganic carbon for photo-synthesis in a strain of Phaeodactylum tricornutum. Limnol Oceanogr 47:1192–1197
Colman B, Hosain ML (1980) The release of glycolate by a fresh-water diatom. J Phycol 16:478–479
Colman B, Rotatore C (1995) Photosynthetic inorganic carbon uptake and accumulation in two marine diatoms. Plant Cell Environ 18:919–924
Colman B, Huerta IE, Bhatti S et al (2002) The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae. Funct Plant Biol 29:261–270
Coombs J, Volcani BE (1968) Studies on the biochemistry and fine structure of silica shell formation in diatoms. Silicon-induced metabolic transients in Navicula pelliculosa (Bréb.) Hilse. Planta 80:264–279
Cox EH, McLendon GL, Morel FMM et al (2000) The active site structure of Thalassiosira weissflogii carbonic anhydrase 1. Biochemistry 39:12128–12130
Derelle E, Ferraz C, Rombauts S et al (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natnl Acad Sci USA 103:11647–11652
Drum RW (1963) The cytoplasmic fine structure of the diatom, Nitzschia palea. J Cell Biol 18:429–440
Drum RW, Pancratz HS (1964) Pyrenoids, raphes, and other fine structure of diatoms. Am J Bot 51:405–418
Edwards GE, Franceschi VR, Vosnesenskaya EV (2004) Single-cell C4 photosynthesis versus dual-cell (Kranz) paradigm. Annu Rev Plant Biol 55:173–196
Eisenhut M, Kahlon S, Hasse D et al (2006) The plant-like C2 glycolate cycle and bacterial-like glycerate pathway cooperate in phosphoglycolate metabolism in cyanobacteria. Plant Physiol 142: 333–342
Enami I, Suzuki T, Tada O et al (2005) Distribution of the extrinsic proteins as a potential marker for the evolution of photosynthetic oxygen-evolving photosystem II. FEBS J 272:5020–5030
Falkowski PG, Katz ME, Knoll AH et al (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360
Field CB, Behrenfeld MJ, Randerson JT et al (1998) Primary production in the ecosphere: integrating terrestrial and oceanic components. Science 281:337–360
Fielding AS, Turpin DH, Guy RD et al (1998) Influence of carbon concentrating mechanism on carbon stable isotope discrimination by the marine diatom Thalassiosira pseudonana. Can J Bot 76:1098–1103
Geider RJ, Osborne BA, Raven JA (1985) Light dependence of growth and photosynthesis in Phaeodactylum tricornutum (Bacillariophyceae). J Phycol 21:609–619
Geider RJ, Osborne BA, Raven JA (1986) Growth, photosynthesis and maintenance metabolic cost in the diatom Phaeodactylum tricornutum at very low light levels. J Phycol 22:39–48
Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131
Granum E, Myklestad SM (1999) Effects of NH +4 assimilation on dark carbon fixation and β-1,3-glucan metabolism in the marine diatom Skeletonema costatum (Bacillariophyceae). J Phycol 35:1191–1199
Granum E, Raven JA, Leegood RC (2005) How do marine diatoms fix 10 billion tonnes of carbon per year? Can J Bot 83:898–908
Hanson DT, Franklin LA, Samuelsson G et al (2003) The Chlamydomonas reinhardtii cia3 mutant lacking a thylakoid lumen-localized carbonic anhydrase is limited by CO2 supply to Rubisco and not photosystem II in vivo. Plant Physiol 132:2267–2275
Harada H, Nakajima K, Sakaue K et al (2006) CO2 sensing at ocean surface mediated by cAMP in a marine diatom. Plant Physiol 142:1318–1328
Hillier W, McConnell I, Badger MR et al (2006) Quantitative assessment of intrinsic carbonic anhydrase activity and capacity for bicarbonate oxidation in photosystem II. Biochemistry 45:2094–2102
Holdsworth ES, Colbeck J (1976) The pattern of carbon fixation in the unicellular alga Phaeodactylum tricornutum. Mar Biol 38:189–199
Holtum JAM, Smith JAC, Neuhaus HE (2005) Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism. Funct Plant Biol 32:429–449
Johnston AM, Raven JA (1996) Inorganic carbon accumulation by the marine diatom Phaeodactylum tricornutum. Eur J Phycol 31:988–990
Johnston AM, Raven JA, Beardall J et al (2001) Photosynthesis in a marine diatom. Nature 412:40–41
Kaczmarska I, Beaton M, Benoit AC et al (2006) Molecular phylogeny of selected members of the order Thalassiosirales (Bacillariophyta) and evolution of the fultoportula. J Phycol 42:121–138
Keeley JE, Rundel PW (2003) Evolution of CAM and C–4 carbon concentrating mechanisms. Int J Plant Physiol 164:S55–S77
Kellog EA (1999) Phylogenetic aspects of the evolution of C4 photosynthesis. In: Sage RF, Monson RL (eds) C4 Plant biology. Academic Press, San Diego, pp 411–444
Kerfeld CA, Saway MR, Tanaka S et al (2005) Protein structures forming the shell of primitive bacterial organelles. Science 309:151–163
Kremer BP, Berks R (1978) Photosynthesis and carbon metabolism in marine and freshwater diatoms. Z Pfl Physiol 87:149–165
Lane TW, Saito MA, Geroget GN et al (2005) A cadmium enzyme from a marine diatom. Nature 435:42
Lee RE, Kugrens P (1998) Hypothesis: the ecological advantage of chloroplast ER–the ability to outcompete at low dissolved CO2 concentrations. Protist 149:341–345
Lee RE, Kugrens P (2000) Ancient atmospheric CO2 and timing of the evolution of secondary endosymbioses. Phycologia 39:167–172
Lu YK, Theg SM, Stemler AJ (2005) Carbonic anhydrase activity of the photosystem II OEC33 protein from pea. Plant Cell Physiol 46:1944–1953
Martin CL, Tortell PD (2006) Bicarbonate transport and extracellular carbonic anhydrase capacity in Bering Sea phytoplankton assemblages: results from isotope disequilibrium experiments. Limnol Oceanogr 51:2111–2121
Matsuda Y, Hara T, Colman B (2001) Regulation of the induction of bicarbonate uptake by dissolved CO2 in the marine diatom, Phaeodactylum tricornutum. Plant Cell Environm 24:611–620
Matsuda Y, Satoh K, Harada H et al (2002) Regulation of the expressions of HCO −3 uptake and intracellular carbonic anhydrase activity in response to CO2 concentration in the marine diatom Phaeodactylum sp. Funct Plant Biol 29:279–287
Mayama S, Mayama N, Shihara-Ishikawa I (2004) Characterization of linear-oblong pyrenoids with cp-DNA along their sides in Nitzschia sigmoidea (Bacillariophyceae). Phycol Res 52:129–139
Mitchell C, Beardall J (1976) Inorganic C uptake by an Antarctic sea-ice diatom Nitzschia frigida. Polar Biology 16:95–99
Mitra M, Mason CB, Xiao Y et al (2005) The carbonic anhydrase gene families of Chlamydomonas reinhardtii. Can J Bot 83:301–308
Monson RK, Moore BD, Ku MSB et al (1986) Co-function of C3- and C4-photosynthetic pathways in C3, C4 and C3 − C4 intermediate Flaveria species. Planta 168:493–502
Montsant A, Jabbari K, Maheswari U et al (2005) Comparative genomics of the pennate diatom Phaeodactylum tricornutum. Plant Physiol 137:500–513
Morel FMM, Cox EH, Kraepiel AML et al (2002) Acquisition of inorganic carbon by the marine diatom Thalassiosira weissflogii. Funct Plant Biol 28:301–308
Mortain-Bertrand A, Descolas-Gros C, Jupin H (1987) Short-term 14C incorporation in Skeletonema costatum (Greville) Cleve (Bacillariophyceae) as a function of light regime. Phycologia 26:262–269
Mortain-Bertrand A, Descolas-Gros C, Jupin H (1998) Pathway of dark inorganic carbon fixation in two species of diatoms—influence of light regime and regulatory factors on diel variations. J Plankton Res 10:199–217
Myers J (1980) On the algae. In: Falkowski PG (ed) Primary productivity in the sea. Plenum Press, New York, pp 1–15
Nimer NA, Brownlee C, Merrett MJ (1999) Extracellular carbonic anhydrase facilitates carbon dioxide availability for photosynthesis in the marine dinoflagellate Prorocentrum micans. Plant Physiol 120:105–111
Park H, Song B, Morel FMM (2007) Diversity of cadmium-containing carbonic anhydrase in marine diatoms and natural waters. Env Microbiol 9:403–413
Parker MS, Armbrust EV, Piovia-Scott J et al (2004) Induction of photorespiration by light in the centric diatom Thalassiosira weissflogii (Bacillariophyceae): molecular characterization and physiological consequences. J Phycol 40:557–567
Parker MS, Armbrust EV (2005) Synergistic effects of light, temperature, and nitrogen source on transcription of genes for carbon and nitrogen metabolism in the centric diatom Thalassiosira pseudonana (Bacillariophyceae). J Phycol 41:1142–1153
Peers G, Price NM (2006) Copper-containing plastocyanin used for electron transport by an oceanic diatom. Nature 441:341–344
Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53:523–555
Pronina NA, Semenenko VE (1992) Role of the pyrenoid in concentration, generation, and fixation of CO2 in the chloroplasts of microalgae. Soviet Plant Physiol 39:470–476
Raven JA (1984) Energetics and transport in aquatic plants. AR Liss, New York
Raven JA (1987) The role of vacuoles. New Phytol 106:357–422
Raven JA (1995) Scaling the seas. Plant Cell Environ 18:1090–1100
Raven JA (1997) CO2 concentrating mechanisms: a direct role for thylakoid lumen acidification? Plant Cell Environm 20:147–154
Raven JA, Spicer RA (1996) The evolution of crassulacean acid metabolism. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution. Springer, Berlin, pp 360–385
Raven JA, Waite AM (2004) The evolution of silicification in diatoms: inescapable sinking and sinking as escape? New Phytol 162:45–61
Raven JA, Kübler JE, Beardall J (2000) Put out the light, and then put out the light. J Mar Biol Assoc UK 80:1–25
Raven JA, Roberts K, Granum E et al (2007) The ecology and evolution of single-cell C4-like photosynthesis in diatoms: Relevance to C4 rice. In: Sheehy J, Mitchell P (eds) Charting new pathways to C4 rice. World Scientific Publishers, Singapore (in press)
Reinfelder JR, Kraepiel AML, Morel FMM (2000) Unicellular C4 photosynthesis in a marine diatom. Nature 407:969–999
Reinfelder JR, Milligan AJ, Morel FMM (2004) The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiol 135:2106–2111
Roberts SB, Lane TW, Morel FMM (1997) Carbonic anhydrase in the marine diatom Thalassiosira weissflogii. J Phycol 33:845–850
Rost B, Riebesell U, Burkhardt S et al (2003) Carbon acquisition by bloom-forming marine phytoplankton. Limnol Oceanogr 48:55–67
Rotatore C, Colman B (1992) Active uptake of CO2 by the diatom Navicula pelliculosa. J Exp Bot 43:571–576
Rotatore C, Colman B, Kuzuma M (1995) The active uptake of carbon dioxide by the marine diatoms Phaeodactylum tricornutum and Cyclotella sp. Plant Cell Environ 18:913–918
Sage RF, Li M, Monson RK (1999) The taxonomic distribution of C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, San Diego, pp 551–584
Satoh D, Hiraoka R, Colman B et al (2001) Physiological and molecular biological characteristics on intracellular carbonic anhydrase from the marine diatom Phaeodactylum tricornutum. Plant Physiol 126:1459–1470
Schmid AM (2001) Value of pyrenoids in the systematics of diatoms: their morphology and ultrastructure. In: Economou-Amilli A (ed) Proceedings of the 16th international diatom symposium. University of Athens Press, Athens, pp 1–32
Shiraiwa Y, Danbara A, Yoke K (2004) Characterization of highly oxygen-sensitive photosynthesis in coccolithophorids. Jap J Phycol 52 (suppl):87–94
Sicko-Goad L, Stoermer EGF, Ladewski BG (1977) A morphometric method for correcting phytoplankton cell volume. Protoplasma 93:1–6
Sicko-Goad L, Stoermer EF (1979) A morphometric study of lead and copper effects on Diatoma tenue var elongatum (Bacillariophyta). J Phycol 15:316–321
Sicko-Goad L, Simmons MS, Lazinsky D et al (1988) Effect of light cycle on diatom fatty acid composition and quantitative morphology. J Phycol 24:1–7
Stemler AJ, Govindjee (1973) Bicarbonate ion as a critical factor in photosynthetic O2 evolution. Plant Physiol 52:119–123
Strzepek RF, Harrison PJ (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431:689–692
Szabo E, Colman B (2007) Isolation and characterization of carbonic anhydrases from the marine diatom Phaeodactylum tricornutum. Physiol Plant 129:484–492
Tanaka Y, Nakatsuma D, Harada H et al (2005) Localization of soluble β-carbonic anhydrase in the marine diatom Phaeodactylum tricornutum. Sorting to the chloroplast and cluster formation on the girdle lamella. Plant Physiol 138:207–217
Tcherkez GGB, Farquhar GD, Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimised. Proc Natl Acad Sci USA 103:7246–7251
Tchernov D, Helman Y, Keren N et al (2001) Passive entry of CO2 and its energy-driven intracellular conversion to HCO −3 in cyanobacteria are driven by a photosystem I-generated Δμ +H . J Biol Chem 276:23450–23455
Tsuji Y, Iwamoto K, Suzuki I et al (2006) A mechanism of photosynthetic carbon fixation in the haptophyte alga, Emiliania huxleyi. Plant Cell Physiol 47(suppl):s53
van Hunnik E, Sültemeyer D (2002) A possible role for carbonic anhydrase in the lumen of chloroplasts in green algae. Funct Plant Biol 29:243–249
Villareal TA, Joseph L, Brezinski MA et al (1999) Biological and chemical characteristics of the giant diatom Ethmodiscus (Bacillariophyceae) in the Central North Pacific Gyre. J Phycol 35:896–902
Walker NA, Smith FA, Cathers IR (1980) Bicarbonate assimilation by freshwater charophytes and higher plants. I Membrane transport of bicarbonate ions is not proven. J Membr Biol 57:51–58
Whitney SM, Baldett O, Hudson GS et al (2001) Form I Rubiscos from non-green algae are expressed abundantly but are not assembled in tobacco chloroplasts. Plant J 26:535–547
Winkler U, Stabenau H (1995) Isolation and characterization of peroxisomes from diatoms. Planta 195:403–407
Wittpoth C, Kroth PG, Weyrauch KV et al (1998) Functional characterization of isolated plastids from two diatoms. Planta 206:79–95
Acknowledgements
Unpublished work reported here was performed under grant NER/A/S/2001/01130 from the Natural Environment Research Council, UK. We are grateful to Professor D G Mann for pointing out the work of Schmid (2001), and to the comments of two anonymous reviewers which have significantly improved the paper.
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Roberts, K., Granum, E., Leegood, R.C. et al. Carbon acquisition by diatoms. Photosynth Res 93, 79–88 (2007). https://doi.org/10.1007/s11120-007-9172-2
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DOI: https://doi.org/10.1007/s11120-007-9172-2