Skip to main content
Log in

A chloroplast pump model for the CO2 concentrating mechanism in the diatom Phaeodactylum tricornutum

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Prior analysis of inorganic carbon (Ci) fluxes in the diatom Phaeodactylum tricornutum has indicated that transport of Ci into the chloroplast from the cytoplasm is the major Ci flux in the cell and the primary driving force for the CO2 concentrating mechanism (CCM). This flux drives the accumulation of Ci in the chloroplast stroma and generates a CO2 deficit in the cytoplasm, inducing CO2 influx into the cell. Here, the “chloroplast pump” model of the CCM in P. tricornutum is formalized and its consistency with data on CO2 and HCO3 uptake rates, carbonic anhydrase (CA) activity, intracellular Ci concentration, intracellular pH, and RubisCO characteristics is assessed. The chloroplast pump model can account for the major features of the data. Analysis of photosynthetic and Ci uptake rates as a function of external Ci concentration shows that the model has the most difficulty obtaining sufficiently low cytoplasmic CO2 concentrations to support observed CO2 uptake rates at low external Ci concentrations and achieving high rates of photosynthesis. There are multiple ways in which model parameters can be varied, within a plausible range, to match measured rates of photosynthesis and CO2 uptake. To increase CO2 uptake rates, CA activity can be increased, kinetic characteristics of the putative chloroplast pump can be enhanced to increase HCO3 export, or the cytoplasmic pH can be raised. To increase the photosynthetic rate, the permeability of the pyrenoid to CO2 can be reduced or RubisCO content can be increased.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Anning T, Nimer N, Merrett MJ, Brownlee C (1996) Costs and benefits of calcification in coccolithophorids. J Marine Syst 9:45–56

    Article  Google Scholar 

  • Badger MR, Palmqvist K, Yu JW (1994) Measurement of CO2 and HCO3 fluxes in cyanobacteria and microalgae during steady-state photosynthesis. Physiol Plantarum 90:529–536

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Braun FJ, Hegemann P (1999) Direct measurement of cytosolic calcium and pH in living Chlamydomonas reinhardtii cells. Eur J Cell Biol 78:199–208

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Burns BD, Beardall J (1987) Utilization of inorganic carbon by marine microalgae. J Exp Mar Biol Ecol 107:75–86

    Article  CAS  Google Scholar 

  • Cassar N, Laws EA, Popp BN, Bidigare RR (2002) Sources of inorganic carbon for photosynthesis in a strain of Phaeodactylum tricornutum. Limnol Oceanogr 47:1192–1197

    Article  Google Scholar 

  • Colman B, Rotatore C (1995) Photosynthetic inorganic carbon uptake and accumulation in two marine diatoms. Plant Cell Environ 18:919–924

    Article  CAS  Google Scholar 

  • Ducklow HW, Harris RP (1993) Introduction to the JGOFS North-Atlantic bloom experiment. Deep Sea Res II 40:1–8

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Harada H, Nakajima K, Sakaue K, Matsuda Y (2006) CO2 sensing at ocean surface mediated by cAMP in a marine diatom. Plant Physiol 142:1318–1328

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Heldt HW, Werdan K, Milovancev M, Geller G (1973) Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. Biochim Biophys Acta 314:224–241

    Article  CAS  PubMed  Google Scholar 

  • Herve V, Derr J, Douady S, Quinet M, Moisan L, Lopez PJ (2012) Multiparametric analyses reveal the pH-dependence of silicon biomineralization in diatoms. PLoS One 7:e46722

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jin X, Gruber N, Dunne JP, Sarmiento JL, Armstrong RA (2006) Diagnosing the contribution of phytoplankton functional groups to the production and export of particulate organic carbon, CaCO3, and opal from global nutrient and alkalinity distributions. Global Biogeochem Cycles. doi:10.1029/2005GB002532

    Google Scholar 

  • Johnson KS (1982) Carbon dioxide hydration and dehydration kinetics in seawater. Limnol Oceanogr 27:849–855

    Article  CAS  Google Scholar 

  • Kikutani S, Tanaka R, Yamazaki Y, Hara S, Hisabori T, Kroth PG, Matsuda Y (2012) Redox regulation of carbonic anhydrases via thioredoxin in chloroplast of the marine diatom Phaeodactylum tricornutum. J Biol Chem 287:20689–20700

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Knauf PA, Law FY, Leung TWV, Gehret AU, Perez ML (2002) Substrate-dependent reversal of anion transport site orientation in the human red blood cell anion-exchange protein, AE1. Proc Natl Acad Sci USA 99:10861–10864

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kramer DM, Sacksteder CA, Cruz JA (1999) How acidic is the lumen? Photosyn Res 60:151–163

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Martino AD, Meichenin A, Shi J, Pan K, Bowler C (2007) Genetic and phenotypic characterization of Phaeodactylum tricornutum (Bacillariophyceae) accessions. J Phycol 43:992–1009

    Article  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nakajima K, Tanaka A, Matsuda Y (2013) SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater. Proc Natl Acad Sci USA 110:1767–1772

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ohno N, Inoue T, Yamashiki R, Nakajima K, Kitahara Y, Ishibashi M, Matsuda Y (2012) CO2-cAMP-responsive cis-elements targeted by a transcription factor with CREB/ATF-like basic zipper domain in the marine diatom Phaeodactylum tricornutum. Plant Physiol 158:499–513

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Price GD, Badger MR (1989) Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC7942 creates a high CO2-requiring phenotype: evidence for a central role for carboxysomes in the CO2 concentrating mechanism. Plant Physiol 91:505–513

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Price NM, Harrison GI, Hering JG, Hudson RJ, Nirel PMV, Palenik B, Morel FMM (1988) Preparation and chemistry of the artificial algal culture medium Aquil. Biol Oceanogr 6:443–462

    Google Scholar 

  • Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101:18228–18233

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raven JA, Smith FA (1978) Effect of temperature and external pH on the cytoplasmic pH of Chara corallina. J Exp Bot 29:853–866

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Romero MF, Boron WF (1999) Electrogenic Na+/HCO3 cotransporters: cloning and physiology. Ann Rev Physiol 61:699–723

    Article  CAS  Google Scholar 

  • Romero MF, Fulton CM, Boron WF (2004) The SLC4 family of HCO3 transporters. Pflug Arch Eur J Physiol 447:495–509

    Article  CAS  Google Scholar 

  • Rost B, Riebesell U, Burkhardt S, Sültemeyer D (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnol Oceanogr 48:55–67

    Article  Google Scholar 

  • Rost B, Kranz SA, Richter KU, Tortell PD (2007) Isotope disequilibrium and mass spectrometric studies of inorganic carbon acquisition by phytoplankton. Limnol Oceanogr-Meth 5:328–337

    Article  CAS  Google Scholar 

  • Satoh D, Hiraoka Y, Colman B, Matsuda Y (2001) Physiological and molecular biological characterization of intracellular carbonic anhydrase from the marine diatom Phaeodactylum tricornutum. Plant Physiol 126:1459

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tachibana M, Allen AE, Kikutani S, Endo Y, Bowler C, Matsuda Y (2011) Localization of putative carbonic anhydrases in two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana. Photosyn Res 109:205–221

    Article  CAS  PubMed  Google Scholar 

  • Tanaka Y, Nakatsuma D, Harada H, Ishida M, Matsuda Y (2005) Localization of soluble β-carbonic anhydrase in the marine diatom Phaeodactylum tricornutum. Sorting to the chloroplast and cluster formation on the girdle lamellae. Plant Physiol 138:207–217

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Whitney SM, Baldet P, Hudson GS, Andrews TJ (2001) Rubiscos from non-green algae are expressed abundantly but not assembled in tobacco chloroplasts. Plant J 26:535–547

    Article  CAS  PubMed  Google Scholar 

  • Zeebe RE, Wolf-Gladrow D (2001) CO2 in seawater: equilibrium, kinetics, isotopes. Elsevier, Amsterdam

    Google Scholar 

  • Zhang HN, Byrne RH (1996) Spectrophotometric pH measurements of surface seawater at in situ conditions: absorbance and protonation behavior of thymol blue. Mar Chem 52:17–25

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Science Foundation (EF 1041023 and MCB 1129326 to B.H.). J. Losh and F.M.M. Morel (Princeton University) are thanked for providing data on total protein and RubisCO content in P. tricornutum. Comments from two anonymous reviewers improved the work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brian M. Hopkinson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hopkinson, B.M. A chloroplast pump model for the CO2 concentrating mechanism in the diatom Phaeodactylum tricornutum . Photosynth Res 121, 223–233 (2014). https://doi.org/10.1007/s11120-013-9954-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-013-9954-7

Keywords

Navigation