Marine Biology

, Volume 154, Issue 3, pp 413–422 | Cite as

Flux capacities and acclimation costs in Trichodesmium from the Gulf of Mexico

  • Christopher M. Brown
  • James D. MacKinnon
  • Amanda M. Cockshutt
  • Tracy A. Villareal
  • Douglas A. CampbellEmail author
Research Article


Phytoplankton function and acclimation are driven by catalytic protein complexes that mediate key physiological transformations, including generation of photosynthetic ATP and reductant, and carbon and nitrogen fixation. Quantitation of capacities for these processes allows estimation of rates for key ecosystem processes, and identification of factors limiting primary productivity. We herein present molar quantitations of PSI, PSII, ATP synthase, RuBisCO and the Fe protein of nitrogenase of Trichodesmium collected from the Gulf of Mexico, in comparison to determinations for a range of cyanobacteria growing in culture. Using these measurements, estimates were generated for Trichodesmium capacities for carbon fixation of 1–3.4 g C g chl a −1 h−1 and nitrogen fixation of 0.06–0.17 g N g chl a −1 h−1, with diel variations in capacities. ATP synthase levels show that ATP synthesis capacity is sufficient to support these levels of carbon and nitrogen fixation, and that ATP synthase levels change over the day in accordance with the ATP demands of nitrogenase and RuBisCO activity. Levels of measured complexes indicate that Trichodesmium manifests n-type diel light acclimation through rapid changes in RuBisCO:PSII, supported by significant investment of cellular nitrogen. The plasticity in the levels and stoichiometry of these core complexes show that changes in the abundance of core protein complexes are an important component of acclimation and regulation of metabolic function by Trichodesmium populations.


RbcL Diel Cycle MoFe Protein RuBisCO Content Diazotrophic Cyanobacterium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by an NSERC Discovery grant and funding from the Canada Research Chair and Canadian Foundation for Innovation to DAC. CMB was the recipient of an NSERC Industrial Postgraduate Scholarship in collaboration with AgriSera AB. AMC was partially supported by the RTI Program of the New Brunswick Innovation Foundation. AgriSera AB ( and Environmental Proteomics NB ( collaborated on the production of immunodetection reagents. We thank Drs. Yannick Huot, Zoe Finkel, Andrew Irwin, Christophe Six and Joanna Porankiewicz-Asplund for discussions. Contribution number 1454 from The University of Texas Marine Science Institute. The research described complies with the current laws of Canada and the United States of America.

Supplementary material

227_2008_933_MOESM1_ESM.doc (58 kb)
Electronic supplementary materials (DOC 57 kb)
227_2008_933_MOESM2_ESM.tif (95 kb)
Fig. S.1 (TIF 95.3 kb)
227_2008_933_MOESM3_ESM.tif (299 kb)
Fig. S.2 (TIF 299 kb)
227_2008_933_MOESM4_ESM.tif (278 kb)
Fig. S.3 (TIF 278 kb)


  1. Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134PubMedCrossRefGoogle Scholar
  2. Behrenfeld MJ, Prasil O, Kolber ZS, Babin M, Falkowski PG (1998) Compensatory changes in Photosystem II electron turnover rates protect photosynthesis from photoinhibition. Photosynth Res 58:259–268CrossRefGoogle Scholar
  3. Bender RA, Janssen KA, Resnick AD, Blumenberg M, Foor F, Magasanik B (1977) Biochemical parameters of glutamine synthetase from Klebsiella aerogenes. J Bacteriol 129:1001–1009PubMedGoogle Scholar
  4. Berman-Frank I, Lundgren P, Chen YB, Kupper H, Kolber Z, Bergman B, Falkowski P (2001) Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294:1534–1537PubMedCrossRefGoogle Scholar
  5. Boussiba S, Richmond AE (1980) C-phycocyanin as a storage protein in the blue-green alga Spirulina platensis. Arch Microbiol 125:143–147CrossRefGoogle Scholar
  6. Campbell DA, Cockshutt AM, Porankiewicz-Asplund J (2003) Analysing photosynthetic complexes in uncharacterized species or mixed microalgal communities using global antibodies. Physiol Plant 119:322–327CrossRefGoogle Scholar
  7. Capone DG (1993) Determination of nitrogenase activity in aquatic samples using the acetylene reduction procedure. In: Kemp PF (eds) Handbook of methods in aquatic microbial ecology. Lewis, Boca Raton, pp 621–631Google Scholar
  8. Capone DG, Oneil JM, Zehr J, Carpenter EJ (1990) Basis for diel variation in nitrogenase activity in the marine planktonic cyanobacterium Trichodesmium-Thiebautii. Appl Environ Microbiol 56:3532–3536PubMedGoogle Scholar
  9. Carpenter EJ, Subramaniam A, Capone DG (2004) Biomass and primary productivity of the cyanobacterium Trichodesmium spp. in the tropical N Atlantic ocean. Deep Sea Res Pt I 51:173–203CrossRefGoogle Scholar
  10. Chen YB, Dominic B, Mellon MT, Zehr JP (1998) Circadian rhythm of nitrogenase gene expression in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. strain IMS 101. J Bacteriol 180:3598–3605PubMedGoogle Scholar
  11. Chen YB, Dominic B, Zani S, Mellon MT, Zehr JP (1999) Expression of photosynthesis genes in relation to nitrogen fixation in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. IMS 101. Plant Mol Biol 41(1):89–104PubMedCrossRefGoogle Scholar
  12. Chitnis PR (2001) Photosystem I: function and physiology. Annu Rev Plant Physiol Plant Mol Biol 52:593–626PubMedCrossRefGoogle Scholar
  13. de Lorimier RM, Smith RL, Stevens SE (1992) Regulation of phycobilisome structure and gene expression by light intensity. Plant Physiol 98:1003–1010PubMedGoogle Scholar
  14. Einsle O, Tezcan FA, Andrade SLA, Schmid B, Yoshida M, Howard JB, Rees DC (2002) Nitrogenase MoFe-protein at 1.16 angstrom resolution: a central ligand in the FeMo-cofactor. Science 297:1696–1700PubMedCrossRefGoogle Scholar
  15. Falkowski P, Owens TG (1980) Light-shade adaptation two strategies in marine phytoplankton. Plant Cell Physiol 66:592–595Google Scholar
  16. Falkowski PG, Raven J (1997) Aquatic photosynthesis. Blackwell, OxfordGoogle Scholar
  17. Fay P, Steward WD, Walsby AE, Fogg GE (1968) Is the heterocyst the site of nitrogen fixation in the blue-green algae? Nature 220:810–812PubMedCrossRefGoogle Scholar
  18. Fischer S, Graber P (1999) Comparison of DeltapH- and Delta***φ***-driven ATP synthesis catalyzed by the H(+)-ATPases from Escherichia coli or chloroplasts reconstituted into liposomes. FEBS Lett 457:327–332PubMedCrossRefGoogle Scholar
  19. Fu FX, Bell PR (2003) Growth, N2 fixation and photosynthesis in a cyanobacterium, Trichodesmium sp., under Fe stress. Biotechnol Lett 25:645–649PubMedCrossRefGoogle Scholar
  20. Fujita Y (1997) A study on the dynamic features of photosystem stoichiometry: Accomplishments and problems for future studies. Photosynth Res 53:83–93CrossRefGoogle Scholar
  21. Geider RJ, MacIntyre HL (2002) Physiology and biochemistry of photosynthesis and algal carbon acquisition. In: Williams PJ, Thomas DN, Reynods CS (eds) Phytoplankton productivity: carbon assimilation in marine and freshwater ecosystems. Blackwell, Oxford, pp 44–77Google Scholar
  22. Groth G, Pohl E (2001) The structure of the chloroplast F1-ATPase at 3.2 a resolution. J Biol Chem 276:1345–1352PubMedCrossRefGoogle Scholar
  23. Hardy RWF, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207PubMedCrossRefGoogle Scholar
  24. Heber U, Neimanis S, Dietz KJ (1988) Fractional control of photosynthesis by the QB protein, the cytochrome f/b6 complex and other components of the photosynthetic apparatus. Planta 173:267–274CrossRefGoogle Scholar
  25. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411:909–917PubMedCrossRefGoogle Scholar
  26. Kok B (1956) On the inhibition of photosynthesis by intense light. Biochim Biophys Acta 21:234–244PubMedCrossRefGoogle Scholar
  27. Kromkamp J (1987) Formation and functional significance of storage products in cyanobacteria. N Z J Mar Freshwater Res 21:457–465CrossRefGoogle Scholar
  28. Kupper H, Ferimazova N, Setlik I, Berman-Frank I (2004) Traffic lights in Trichodesmium. Regulation of photosynthesis for nitrogen fixation studied by chlorophyll fluorescence kinetic microscopy. Plant Physiol 135:2120–2133PubMedCrossRefGoogle Scholar
  29. Lawlor DW, Boyle FA, Young AT, Keys AJ, Kendall AC (1987) Nirate nutrition and temperature effects on wheat: photosynthesis and photorespiration of leaves. J Exp Bot 38:393–408CrossRefGoogle Scholar
  30. Leverenz JW, Falk S, Pilstrom CM, Samuelsson G (1990) The effects of photoinhibition on the photosynthetic light-response curve of green plant-cells (Chlamydomonas-reinhardtii). Planta 182:161–168CrossRefGoogle Scholar
  31. Lilley RM, Walker DA (1974) An improved spectrophotometric assay for ribulosebisphosphate carboxylase. Biochim Biophys Acta 358:226–229PubMedGoogle Scholar
  32. Lin S, Henze S, Lundgren P, Bergman B, Carpenter EJ (1998) Whole-cell immunolocalization of nitrogenase in marine diazotrophic cyanobacteria, Trichodesmium spp. Appl Environ Microbiol 64:3052–3058PubMedGoogle Scholar
  33. Liu H., Dagg MJ (2003) Interactions between nutrients, phytoplankton growth, and micro- and meso-zooplankton grazing in the plume of the Mississippi River. Mar Ecol Prog Ser 258:31–42CrossRefGoogle Scholar
  34. MacKenzie TDB, Burns RA, Campbell DA (2004) Carbon status constrains light acclimation in the cyanobacterium Synechococcus elongatus. Plant Physiol 136:3301–3312PubMedCrossRefGoogle Scholar
  35. Malinsky-Rushansky N, Berman T, Berner T, Yacobi YZ, Dubinsky Z (2002) Physiological characteristics of picophytoplankton, isolated from Lake Kinneret: responses to light and temperature. J Plankton Res 24:1173–1183CrossRefGoogle Scholar
  36. Marcus Y, Gurevitz M (2000) Activation of cyanobacterial RuBP-carboxylase/oxygenase is facilitated by inorganic phosphate via two independent mechanisms. Eur J Biochem 267:5995–6003PubMedCrossRefGoogle Scholar
  37. Marcus Y, Altman-Gueta H, Finkler A, Gurevitz M (2003) Dual role of cysteine 172 in redox regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase activity and degradation. J Bacteriol 185:1509–1517PubMedCrossRefGoogle Scholar
  38. McCarthy J, Carpenter EJ (1979) Oscillatoria (Trichodesmium) thiebautii (Cyanophyta) in the central north Atlantic Ocean. J Phycol 15:75–82CrossRefGoogle Scholar
  39. Meeks JC, Wolk CP, Thomas J, Lockau W, Shaffer PW, Austin SM, Chien WS, Galonsky A (1977) The pathways of assimilation of 13NH4+ by the cyanobacterium, Anabaena cylindrica. J Biol Chem 252:7894–7900PubMedGoogle Scholar
  40. Metzger SU, Cramer WA, Whitmarsh J (1997) Critical analysis of the extinction coefficient of chloroplast cytochrome f. Biochim Biophys Acta 1319:233–241PubMedCrossRefGoogle Scholar
  41. Morell MK, Paul K, O’Shea NJ, Kane HJ, Andrews TJ (1994) Mutations of an active site threonyl residue promote beta elimination and other side reactions of the enediol intermediate of the ribulosebisphosphate carboxylase reaction. J Biol Chem 269:8091–8098PubMedGoogle Scholar
  42. Newman J, Gutteridge S (1993) The X-ray structure of Synechococcus ribulose-bisphosphate carboxylase oxygenase-activated quaternary complex at 2.2-Angstrom resolution. J Biol Chem 268:25876–25886PubMedGoogle Scholar
  43. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749PubMedCrossRefGoogle Scholar
  44. Orellana MV, Perry MJ (1992) An immunoprobe to measure Rubisco concentrations and maximal photosynthesis rates of individual phytoplankton cells. Limnol Oceanogr 37:978–990CrossRefGoogle Scholar
  45. Park YI, Chow WS, Anderson JM (1995) Light inactivation of functional photosystem II in leaves of peas grown in moderate light depends on photon exposure. Planta 196:401–411CrossRefGoogle Scholar
  46. Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156PubMedCrossRefGoogle Scholar
  47. Rivkin RB (1990) Photoadaptation in marine phytoplankton: variations in ribulose 1,5-bisphosphate activity. Mar Ecol Prog Ser 62:61–72CrossRefGoogle Scholar
  48. Shapiro BM, Stadtman ER (1970) Glutamine synthetase (Escherichia coli). Methods Enzymol 17A:910–922Google Scholar
  49. Shimabukuro K, Yasuda R, Muneyuki E, Hara KY, Kinosita K Jr, Yoshida M (2003) Catalysis and rotation of F1 motor: cleavage of ATP at the catalytic site occurs in 1 ms before 40 degree substep rotation. Proc Natl Acad Sci USA 100:14731–14736PubMedCrossRefGoogle Scholar
  50. Simpson FB, Burris RH (1984) A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science 224:1095–1097PubMedCrossRefGoogle Scholar
  51. Six C, Worden AZ, Rodriguez F, Moreau H, Partensky F (2005) New insights into the nature and phylogeny of prasinophyte antenna proteins: Ostreococcus tauri, a case study. Mol Biol Evol 22:2217–2230PubMedCrossRefGoogle Scholar
  52. Six C, Finkel ZV, Rodriguez F, Marie D, Partensky F, Campbell DA (2008) Contrasting photoacclimation strategies in oceanic and lagoon ecotypes of the eukaryotic picoplankter Ostreococcus. Limnol Oceanogr 53:255–265Google Scholar
  53. Strop P, Takahara PM, Chiu HJ, Angove HC, Burgess BK, Rees DC (2001) Crystal structure of the all-ferrous [4Fe-4S](0) form of the nitrogenase iron protein from Azotobacter vinelandii. Biochemistry US 40:651–656CrossRefGoogle Scholar
  54. Subramaniam A, Carpenter EJ, Karentz D, Falkowski P (1999) Bio-optical properties of the marine diazotrophic cyanobacteria Trichodesmium spp. I. Absorption and photosynthetic action spectra. Limnol Oceanogr 44:608–617CrossRefGoogle Scholar
  55. Sukenik A, Bennett J, Falkowski PG (1987) Light-saturated photosynthesis—limitation by electron transport or carbon fixation? Biochim Biophys Acta 891:205–215CrossRefGoogle Scholar
  56. Tcherkez GG, 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 103:7246–7251PubMedCrossRefGoogle Scholar
  57. Tomashek JJ, Glagoleva OB, Brusilow WS (2004) The Escherichia coli F1F0 ATP synthase displays biphasic synthesis kinetics. J Biol Chem 279:4465–4470PubMedCrossRefGoogle Scholar
  58. Vichitphan K (2001) Azotobacter vinelandii nitrogenase: effect of amino-acid substitutions at the alpha Gln-191 residue of the MoFe protein on substrate reduction and CO inhibition. Doctor of Philosophy. Biochemistry-US, BlacksburgGoogle Scholar
  59. Weinbaum SA, Gressel J, Reisfeld A, Edelman M (1979) Characterization of the 32,000 Dalton chloroplast membrane protein: probing its biological function in Spirodela. Plant Physiol 64:828–832PubMedGoogle Scholar
  60. Wong PP, Burris RH (1972) Nature of oxygen inhibition of nitrogenase from Azotobacter vinelandii. Proc Natl Acad Sci USA 69:672–675PubMedCrossRefGoogle Scholar
  61. Wyman M, Zehr JP, Capone DG (1996) Temporal variability in nitrogenase gene expression in natural populations of the marine cyanobacterium Trichodesmium thiebautii. Appl Environ Microbiol 62:1073–1075PubMedGoogle Scholar
  62. Yokota A, Canvin DT (1985) Ribulose bisphosphate carboxylase/oxygenase content determined with [14C]carboxypentitol bisphosphate in plants and algae. Plant Physiol 77:735–739PubMedGoogle Scholar
  63. Zehr JP, Wyman M, Miller V, Duguay L, Capone DG (1993) Modification of the Fe protein of nitrogenase in natural populations of Trichodesmium thiebautii. Appl Environ Microbiol 59:669–676PubMedGoogle Scholar
  64. Zehr JP, Waterbury JB, Turner PJ, Montoya JP, Omoregie E, Steward GF, Hansen A, Karl DM (2001) Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412:635–638PubMedCrossRefGoogle Scholar
  65. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Christopher M. Brown
    • 1
    • 2
  • James D. MacKinnon
    • 2
  • Amanda M. Cockshutt
    • 2
  • Tracy A. Villareal
    • 3
  • Douglas A. Campbell
    • 2
    Email author
  1. 1.Department of BiologyUniversity of New BrunswickFrederictonCanada
  2. 2.Department of BiologyMount Allison UniversitySackvilleCanada
  3. 3.Marine Science InstituteThe University of Texas at AustinPort AransasUSA

Personalised recommendations