Photosynthesis Research

, Volume 124, Issue 1, pp 45–56

Electron transport kinetics in the diazotrophic cyanobacterium Trichodesmium spp. grown across a range of light levels

  • Xiaoni Cai
  • Kunshan Gao
  • Feixue Fu
  • Douglas A. Campbell
  • John Beardall
  • David A. Hutchins
Regular Paper

Abstract

The diazotrophic cyanobacterium Trichodesmium is a major contributor to marine nitrogen fixation. We analyzed how light acclimation influences the photophysiological performance of Trichodesmium IMS101 during exponential growth in semi-continuous nitrogen fixing cultures under light levels of 70, 150, 250, and 400 μmol photons m−2 s−1, across diel cycles. There were close correlations between growth rate, trichome length, particulate organic carbon and nitrogen assimilation, and cellular absorbance, which all peaked at 150 μmol photons m−2 s−1. Growth rate was light saturated by about 100 μmol photons m−2 s−1 and was photoinhibited above 150 μmol photons m−2 s−1. In contrast, the light level (Ik) to saturate PSII electron transport (e PSII−1 s−1) was much higher, in the range of 450–550 μmol photons m−2 s−1, and increased with growth light. Growth rate correlates with the absorption cross section as well as with absorbed photons per cell, but not to electron transport per PSII; this disparity suggests that numbers of PSII in a cell, along with the energy allocation between two photosystems and the state transition mechanism underlie the changes in growth rates. The rate of state transitions after a transfer to darkness increased with growth light, indicating faster respiratory input into the intersystem electron transport chain.

Keywords

Light Electron transport Trichodesmium State transition 

Abbreviations

PAR

Photosynthetically active radiation (400–700 nm)

PSII

Photosystem II

PSI

Photosystem I

PBS

Phycobilisome

PQ

Plastoquinone

PUB

Phycourobilin

PEB

Phycoerythrobilin

PEC

Phycoerythrocyanin

PC

Phycocyanin

ETR

Electron transport rate

POC

Particulate organic carbon

PON

Particulate organic nitrogen

References

  1. Allen JF, Holmes NG (1986) A general model for regulation of photosynthetic unit function by protein phosphorylation. FEBS Lett 202:175–181Google Scholar
  2. Andresen E, Lohscheider J, Setlikova E, Adamska I, Simek M, Küpper H (2010) Acclimation of Trichodesmium erythraeum ISM101 to high and low irradiance analysed on the physiological, biophysical and biochemical level. New Phytol 185:173–188CrossRefPubMedGoogle Scholar
  3. Berman-Frank I, Lundgren P, Chen YB, Küpper H, Kolber Z, Bergman B, Falkowski P (2001) Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294:1534–1537Google Scholar
  4. Bernát G, Schreiber U, Sendtko E, Stadnichuk IN, Rexroth S, Rögner M, Koenig F (2012) Unique properties vs. common themes: the atypical cyanobacterium Gloeobacter violaceus PCC 7421 is capable of state transitions and blue-light-induced fluorescence quenching. Plant Cell Physiol 53:528–542CrossRefPubMedGoogle Scholar
  5. Breitbarth E, Wohlers J, Kläs J, LaRoche J, Peeken I (2008) Nitrogen fixation and growth rates of Trichodesmium IMS-101 as a function of light intensity. Mar Ecol Prog Ser 359:25–36Google Scholar
  6. Bruce D, Brimble S, Bryant DA (1989) State transitions in a phycobilisome-less mutant of the cyanobacterium Synechococcus sp. PCC 7002. Biochim Biophys Acta 974:66–73Google Scholar
  7. Campbell D, Hurry V, Clarke AK, Gustafsson P, Oquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62:667–683PubMedCentralPubMedGoogle Scholar
  8. Capone D, Zehr J, Paerl H, Bergman B (1997) Trichodesmium, a globally significant marine cyanobacterium. Science 276:1221–1227CrossRefGoogle Scholar
  9. Carpenter E, Roenneberg T (1995) The marine planktonic cyanobacteria Trichodesmium spp.: photosynthetic rate measurements in the SW Atlantic Ocean. Mar Ecol Prog Ser 118:267–273CrossRefGoogle Scholar
  10. Carpenter EJ, Judith M, Capone DG (1993) The tropical diazotrophic phytoplankter Trichodesmium: biological characteristics of two common species. Mar Ecol Prog Ser 95:295–304CrossRefGoogle Scholar
  11. Chen YB, Zehr JP, Mellon M (1996) Growth and nitrogen fixation of the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. IMS101 in defined media: evidence for a circadian rhythm. J Phycol 32:916–923CrossRefGoogle Scholar
  12. Ciotti AM, Lewis MR, Cullen JJ (2002) Assessment of the relationships between dominant cell size in natural phytoplankton communities and the spectral shape of the absorption coefficient. Limnol Oceanogr 47:404–417CrossRefGoogle Scholar
  13. Cleveland JS, Weidemann AD (1993) Quantifying absorption by aquatic particles: a multiple scattering correction for glass-fiber. Limnol Oceanogr 38:1321–1327CrossRefGoogle Scholar
  14. Dubinsky Z, Falkowski PG, Wyman K (1986) Light harvesting and utilization by phytoplankton. Plant Cell Physiol 27:1335–1349Google Scholar
  15. Dugdale R, Menzel DW, Ryther JH (1961) Nitrogen fixation in the Sargasso Sea. Deep-Sea Res 7:297–300Google Scholar
  16. Falkowski PG, Owens TG (1980) Light-shade adaptation. Two strategies in marine phytoplankton. Plant Physiol 66:592–595CrossRefPubMedCentralPubMedGoogle Scholar
  17. Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, New Jersey, pp 237–246Google Scholar
  18. Fujita Y (1997) A study on the dynamic features of photosystem stoichiometry: accomplishments and problems for future studies. Photosynth Res 53:83–93CrossRefGoogle Scholar
  19. Gallon JR (1992) Tansley Review No. 44. Reconciling the incompatible: N2 fixation and O2. New Phytol 122:571–609CrossRefGoogle Scholar
  20. Garcia NS, Fu F-X, Breene CL, Bernhardt PW, Mulholland MR, Sohm JA, Hutchins DA (2011) Interactive effects of irradiance and CO2 on CO2 fixation and N2 fixation in the diazotroph Trichodesmium erythraeum (cyanobacteria). J Phycol 47:1292–1303CrossRefGoogle Scholar
  21. Glibert PM, Bronk DA (1994) Release of dissolved organic nitrogen by marine diazotrophic cyanobacteria, Trichodesmium spp. Appl Environ Microbiol 60:3996–4000PubMedCentralPubMedGoogle Scholar
  22. Goebel NL, Edwards CA, Carter BJ, Achilles KM, Zehr JP (2008) Growth and carbon content of three different-sized diazotrophic cyanobacteria observed in the subtropical North Pacific. J Phycol 44:1212–1220CrossRefGoogle Scholar
  23. Huot Y, Babin M (2010) Overview of fluorescence protocols: theory, basic concepts, and practice. Chlorophyll a fluorescence in aquatic sciences: methods and applications, vol 4. Springer, Berlin, pp 31–74CrossRefGoogle Scholar
  24. Joshua S, Mullineaux CW (2004) Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol 135:2112–2119Google Scholar
  25. Kana TM (1993) Rapid oxygen cycling in Trichodesmium thiebautii. Limnol Oceanogr 38:18–24CrossRefGoogle Scholar
  26. Kolber ZS, Prasil OP, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367:88–106CrossRefPubMedGoogle Scholar
  27. Küpper 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 135:2120–2133CrossRefPubMedCentralPubMedGoogle Scholar
  28. Küpper H, Andresen E, Wiegert S, Simek M, Leitenmaier B, Setlik I (2009) Reversible coupling of individual phycobiliprotein isoforms during state transitions in the cyanobacterium Trichodesmium analysed by single-cell fluorescence kinetic measurements. Biochim Biophys Acta 1787:155–167CrossRefPubMedGoogle Scholar
  29. LaRoche J, Breitbarth E (2005) Importance of the diazotrophs as a source of new nitrogen in the ocean. J Sea Res 53:67–91CrossRefGoogle Scholar
  30. Levitan O, Rosenberg G, Setlik I, Setlikova E, Grigel J, Klepetar J, Prasil O, Berman-Frank I (2007) Elevated CO2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob Change Biol 13:531–538CrossRefGoogle Scholar
  31. Levitan O, Kranz SA, Spungin D, Prasil O, Rost B, Berman-Frank I (2010) Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: a mechanistic view. Plant Physiol 154:346–356CrossRefPubMedCentralPubMedGoogle Scholar
  32. Lewis MR, Ulloa O, Platt T (1988) Photosynthetic action, absorption, and quantum yield spectra for a natural population of Oscillatoria in the North Atlantic. Limnol Oceanogr 33:92–98CrossRefGoogle Scholar
  33. MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curve and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38CrossRefGoogle Scholar
  34. Mao H-B, Li G-F, Ruan X, Wu Q-Y, Gong Y-D, Zhang X-F, Zhao N-M (2002) The redox state of plastoquinone pool regulates state transitions via cytochrome b 6 f complex in Synechocystis sp. PCC 6803. FEBS Lett 519:82–86CrossRefPubMedGoogle Scholar
  35. McConnell MD, Koop R, Vasil’ev S, Bruce D (2002) Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria. A structure-based model for the light state transition. Plant Physiol 130:1201–1212CrossRefPubMedCentralPubMedGoogle Scholar
  36. Mitchell BG (1990) Algorithms for determining the absorption coefficient for aquatic particulates using the quantitative filter technique. In: Proceedings of SPIE 1302, Ocean Optics X, p 137Google Scholar
  37. Mulholland MR, Bernhardt PW (2005) The effect of growth rate, phosphorus concentration, and temperature on N2 fixation, carbon fixation, and nitrogen release in continuous cultures of Trichodesmium IMS101. Limnol Oceanogr 50:839–849CrossRefGoogle Scholar
  38. Mullineaux CW (2014a) Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim Biophys Acta 1837:503–511CrossRefPubMedGoogle Scholar
  39. Mullineaux CW (2014b) Electron transport and light-harvesting switches in cyanobacteria. Front Plant Sci 5:7CrossRefPubMedCentralPubMedGoogle Scholar
  40. Mullineaux CW, Allen JF (1986) The state 2 transition in the cyanobacterium Synechococcus 6301 can be driven by respiratory electron flow into the plastoquinone pool. FEBS Lett 205:155–160CrossRefGoogle Scholar
  41. Mullineaux CW, Allen JF (1990) State 1–State 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between Photosystems I and II. Photosynth Res 23:297–311CrossRefPubMedGoogle Scholar
  42. Mullineaux CW, Holzwarth AR (1990) A proportion of photosystem II core complexes are decoupled from the phycobilisome in light-state 2 in the cyanobacterium Synechococcus 6301. FEBS Lett 260:245–248CrossRefGoogle Scholar
  43. Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701Google Scholar
  44. Richardson K, Beardall J, Raven J (1983) Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytol 93:157–191CrossRefGoogle Scholar
  45. Richier S, Macey AI, Pratt NJ, Honey DJ, Moore CM, Bibby TS (2012) Abundances of iron-binding photosynthetic and nitrogen-fixing proteins of Trichodesmium both in culture and in situ from the North Atlantic. PLoS One 7:e35571CrossRefPubMedCentralPubMedGoogle Scholar
  46. Ritchie RJ (2006) Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res 89:27–41CrossRefPubMedGoogle Scholar
  47. Sandh G, Xu L, Bergman B (2012) Diazocyte development in the marine diazotrophic cyanobacterium Trichodesmium. Microbiology 158:345–352CrossRefPubMedGoogle Scholar
  48. Sarcina M, Tobin MJ, Mullineaux CW (2001) Diffusion of phycobilisomes on the thylakoid membranes of the cyanobacterium Synechococcus 7942: effects of phycobilisome size, temperature, and membrane lipid composition. J Biol Chem 276:46830–46834Google Scholar
  49. Sherman LA, Meunier P, Colón-López MS (1998) Diurnal rhythms in metabolism: a day in the life of a unicellular, diazotrophic cyanobacterium. Photosynth Res 58:25–42Google Scholar
  50. Subramaniam A, Carpenter EJ, Karentz D, Falkowski PG (1999) Bio-optical properties of the marine diazotrophic cyanobacteria Trichodesmium spp. Limnol Oceanogr 44:608–617Google Scholar
  51. van Thor JJ, Mullineaux CW, Matthijs HCP, Hellingwerf KJ (1998) Light harvesting and state transitions in cyanobacteria. Bot Acta 111:430–443Google Scholar
  52. Villareal T (1995) Abundance and photosynthetic characteristics of Trichodesmium spp. along the Atlantic Barrier Reef at Carrie Bow Cay, Belize. Mar Ecol 16:259–271CrossRefGoogle Scholar
  53. Zehr JP (2011) Nitrogen fixation by marine cyanobacteria. Trends Microbiol 19:162–173CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Xiaoni Cai
    • 1
  • Kunshan Gao
    • 1
  • Feixue Fu
    • 2
  • Douglas A. Campbell
    • 3
  • John Beardall
    • 4
  • David A. Hutchins
    • 2
  1. 1.State Key Laboratory of Marine Environmental ScienceXiamen UniversityXiamenChina
  2. 2.Department of Biological SciencesUniversity of Southern CaliforniaLos AngelesUSA
  3. 3.Department of BiologyMount Allison UniversitySackvilleCanada
  4. 4.School of Biological SciencesMonash UniversityClaytonAustralia

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