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Photosystem II cycle activity and alternative electron transport in the diatom Phaeodactylum tricornutum under dynamic light conditions and nitrogen limitation

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Abstract

Alternative electron sinks are an important regulatory mechanism to dissipate excessively absorbed light energy particularly under fast changing dynamic light conditions. In diatoms, the cyclic electron transport (CET) around Photosystem II (PS II) is an alternative electron transport pathway (AET) that contributes to avoidance of overexcitation under high light illumination. The combination of nitrogen limitation and high-intensity irradiance regularly occurs under natural conditions and is expected to force the imbalance between light absorption and the metabolic use of light energy. The present study demonstrates that under N limitation, the amount of AET and the activity of CETPSII in the diatom Phaeodactylum tricornutum were increased. Thereby, the activity of CETPSII was linearly correlated with the amount of AET rates. It is concluded that CETPSII significantly contributes to AET in P. tricornutum. Surprisingly, CETPSII was found to be activated already at the end of the dark period under N-limited conditions. This coincided with a significantly increased degree of reduction of the plastoquinone (PQ) pool. The analysis of the macromolecular composition of cells of P. tricornutum under N-limited conditions revealed a carbon allocation in favor of carbohydrates during the light period and their degradation during the dark phase. A possible linkage between the activity of CETPSII and degree of reduction of the PQ pool on the one side and the macromolecular changes on the other is discussed.

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Abbreviations

AET:

Alternative electron transport

CETPSII :

Cyclic electron transport around Photosystem II

NPQ:

Non-photochemical quenching

PQ:

Plastoquinone

SL:

Sinusoidal light

References

  • Allen AE (2005) Defining the molecular basis for energy balance in marine diatoms under fluctuating environmental conditions. J Phycol 41:1073–1076

    Article  CAS  Google Scholar 

  • Allen AE, Dupont CL, Oborník M, Horák A, Nunes-Nesi A, McCrow JP, Zheng H, Johnson DA, Hu H, Fernie AR, Bowler C (2011) Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473:203–207

    Article  CAS  PubMed  Google Scholar 

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brezinski MA et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

    Article  CAS  PubMed  Google Scholar 

  • Bender SJ, Parker MS, Armbrust EV (2012) Coupled effects of light and nitrogen source on the urea cycle and nitrogen metabolism over a diel cycle in the marine diatom Thalassiosira pseudonana. Protist 163:232–251

    Article  CAS  PubMed  Google Scholar 

  • Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244

    Article  CAS  PubMed  Google Scholar 

  • Bradbury M, Baker NR (1984) A quantitative determination of photochemical and non-photochemical quenching during the slow phase of the chlorophyll fluorescence induction curve of bean leaves. Biochim Biophys Acta 765:275–281

  • Breuer G, Lamers PP, Martens DE, Draaisma RB, Wijffels RH (2012) The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresour Technol 124:217–226

    Article  CAS  PubMed  Google Scholar 

  • Chauton MS, Olsen Y, Vadstein O (2013) Biomass production from the microalga Phaeodactylum tricornutum: nutrient stress and chemical composition in exponential fed-batch cultures. Biomass Bioenergy 58:87–94

    Article  CAS  Google Scholar 

  • Claquin P, Kromkamp JC, Martin-Jezequel V (2004) Relationship between photosynthetic metabolism and cell cycle in a synchronized culture of the marine alga Cylindrotheca fusiformis (Bacillariophyceae). Eur J Phycol 39:33–41

    Article  CAS  Google Scholar 

  • Cleveland JS, Perry MJ (1987) Quantum yield, relative specific absorption and fluorescence in nitrogen-limited Chaetoceros gracilis. Mar Biol 94:489–497

    Article  CAS  Google Scholar 

  • Cruz S, Goss R, Wilhelm C, Leegood R, Horton P, Jakob T (2011) Impact of chlororespiration on non-photochemical quenching of chlorophyll fluorescence and on the regulation of the diadinoxanthin cycle in the diatom Thalassiosira pseudonana. J Exp Bot 62:509–519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Martino A, 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 

  • Dijkman NA, Kroon BMA (2002) Indications for chlororespiration in relation to light regime in the marine diatom Thalassiosira weissflogii. J Photochem Photobiol B 66:179–187

    Article  CAS  PubMed  Google Scholar 

  • Dimier C, Corato F, Tramontano F, Brunet C (2007) Photoprotection and xanthophyll-cycle activity in three marine diatoms. J Phycol 43:937–947

    Article  CAS  Google Scholar 

  • Eisenstadt D, Ohad I, Keren N, Kaplan A (2008) Changes in the photosynthetic reaction centre II in the diatom Phaeodactylum tricornutum result in non-photochemical fluorescence quenching. Environ Microbiol 10:1997–2007

    Article  CAS  PubMed  Google Scholar 

  • Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360

    Article  CAS  PubMed  Google Scholar 

  • Feikema WO, Marosvölgyi MA, Lavaud J, van Gorkom HJ (2006) Cyclic electron transfer in photosystem II in the marine diatom Phaeodactylum tricornutum. Biochim Biophys Acta 1757:829–834

    Article  CAS  Google Scholar 

  • Foy RH, Smith RV (1980) The role of carbohydrate accumulation in the growth of planktonic Oscillatoria species. Brit Phycol J 15:139–150

    Article  Google Scholar 

  • Geider RJ, MacIntyre HL, Graziano LM, McKay RML (1998) Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation. Eur J Phycol 33:315–332

    Article  Google Scholar 

  • Giordano M, Chen Y-B, Koblizek M, Falkowski PG (2005) Regulation of nitrate reductase in Chlamydomonas reinhardtii by the redox state of the plastoquinone pool. Eur J Phycol 40:345–352

    Article  CAS  Google Scholar 

  • Goss R, Jakob T (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth Res 106:103–122

  • Grouneva I, Jakob T, Wilhelm C, Goss R (2009) The regulation of xanthophyll cycle activity and of non-photochemical fluorescence quenching by two alternative electron flows in the diatoms Phaeodactylum tricornutum and Cyclotella meneghiniana. Biochim Biophys Acta 1787:929–938

    Article  CAS  PubMed  Google Scholar 

  • Guerra LT, Levitan O, Frada MJ, Sun JS, Falkowski PG, Dismukes GC (2013) Regulatory branch points affecting protein and lipid biosynthesis in the diatom Phaeodactylum tricornutum. Biomass Bioenergy 59:306–315

    Article  CAS  Google Scholar 

  • Jakob T, Wagner H, Stehfest K, Wilhelm C (2007) A complete energy balance from photons to new biomass reveals a light- and nutrient-dependent variability in the metabolic costs of carbon assimilation. J Exp Bot 58:2101–2112

    Article  CAS  PubMed  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194

    CAS  Google Scholar 

  • Joliot P (2003) Period-four oscillations of the flash-induced oxygen formation in photosynthesis. Photosynth Res 76:65–72

    Article  CAS  PubMed  Google Scholar 

  • Joliot P, Joliot A (1968) A polarographic method for detection of oxygen production and reduction of Hill reagent by isolated chloroplasts. Biochim Biophys Acta 153:625–634

    Article  CAS  PubMed  Google Scholar 

  • Jungandreas A, Schellenberger Costa B, Jakob T, von Bergen M, Baumann S, Wilhelm C (2014) The acclimation of Phaeodactylum tricornutum to blue and red light does not influence the photosynthetic light reaction but strongly disturbs the carbon allocation pattern. PLoS ONE 9:e99727

    Article  PubMed  PubMed Central  Google Scholar 

  • Kroon BMA, Thoms S (2006) From electron to biomass: a mechanistic model to describe phytoplankton photosynthesis and steady-state growth rates. J Phycol 42:593–609

    Article  CAS  Google Scholar 

  • Kroon BMA, Hes UM, Mur LR (1992) An algal cyclostat with computer-controlled dynamic light regime. Hydrobiologia 238:63–70

    Article  Google Scholar 

  • Lavaud J (2007) Fast regulation of photosynthesis in diatoms: mechanisms, evolution and ecophysiology. Funct Plant Sci Biotechnol 1:267–287

    Google Scholar 

  • Lavaud J, Goss R (2014) The peculiar features of non-photochemical fluorescence quenching in diatoms and brown algae. In: Demmig-Adams B, Garab G, III WA, Govindjee (eds.) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Springer, The Netherlands, pp 421–443

  • Lavaud J, van Gorkom H, Etienne A-L (2002) Photosystem II electron transfer cycle and chlororespiration in planktonic diatoms. Photosynth Res 74:51–59

    Article  CAS  PubMed  Google Scholar 

  • Lippemeier S, Hintze R, Vanselow K, Hartig P, Colijn F (2001) In-line recording of PAM fluorescence of phytoplankton cultures as a new tool for studying effects of fluctuating nutrient supply on photosynthesis. Eur J Phycol 36:89–100

    Article  Google Scholar 

  • Lomas MW, Glibert PM (1999) Temperature regulation of nitrate uptake: a novel hypothesis about nitrate uptake and reduction in cool-water diatoms. Limnol Oceanogr 44:556–572

    Article  CAS  Google Scholar 

  • Miyake C, Okamura M (2003) Cyclic electron flow within PSII protects PSII from its photoinhibition in thylakoid membranes from spinach chloroplasts. Plant Cell Physiol 44:457–462

    Article  CAS  PubMed  Google Scholar 

  • Mus F, Toussaint J-P, Cooksey KE, Fields MW, Gerlach R, Peyton BM, Carlson RP (2013) Physiological and molecular analysis of carbon source supplementation and pH stress-induced lipid accumulation in the marine diatom Phaeodactylum tricornutum. Appl Microbiol Biotechnol 97:3625–3642

    Article  CAS  PubMed  Google Scholar 

  • Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components – calculation of qP and F v′/F m′ without measuring F o′. Photosynth Res 54:135–142

    Article  CAS  Google Scholar 

  • Plumley FG, Darley WM (1985) Interactions of light/dark cycles and nitrogen pulses on the timing of cell division in the nitrogen-limited marine diatom Cylindrotheca fusiformis (Bacillariophyceae). J Phycol 21:25–34

    Article  Google Scholar 

  • Provasoli L, McLaughlin JJA, Droop MR (1957) The development of artificial media for marine algae. Arch Mikrobiol 25:392–428

    Article  CAS  PubMed  Google Scholar 

  • Raven JA, Geider RJ (2003) Adaptation, acclimation and regulation in algal photosynthesis. In: Larkum AWD, Douglas SE, Raven JA (eds.) Photosynthesis in Algae. Springer, The Netherlands, pp 385–412

  • Rosenwasser S, van Creveld SG, Schatz D, Malitsky S, Tzfadia O, Aharoni A, Levin Y, Gabashvili A, Feldmesser E, Vardi A (2014) Mapping the diatom redox-sensitive proteome provides insight into response to nitrogen stress in the marine environment. PNAS 111:2740–2745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schansker G, Tóth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta 1706:250–261

    Article  CAS  PubMed  Google Scholar 

  • Schreiber U, Neubauer C (1990) O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res 25:279–293

    Article  CAS  PubMed  Google Scholar 

  • Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Ecophysiology of photosynthesis. Springer, Berlin Heidelberg, pp 49–70

  • Schumann A, Goss R, Jakob T, Wilhelm C (2007) Investigation of the quenching efficiency of diatoxanthin in cells of Phaeodactylum tricornutum (Bacillariophyceae) with different pool sizes of xanthophyll cycle pigments. Phycologia 46:113–117

    Article  Google Scholar 

  • Srivastava A, Strasser RJ, Govindjee (1995) Polyphasic rise of chlorophyll a fluorescence in herbicide-resistant D1 mutants of Chlamydomonas reinardtii. Photosynth Res 43:131–141

    Article  CAS  PubMed  Google Scholar 

  • Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42

    Article  CAS  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the Chlorophyll a Fluorescence Transient. In: Papageorgiou GC, Govindjee (eds.) Chlorophyll a Fluorescence, Springer, The Netherlands, pp 321–362

  • Thomas WH, Seibert DLR, Alden M, Neori A, Eldridge P (1984) Yields, photosynthetic efficiencies and proximate composition of dense marine microalgal cultures. I. Introduction and Phaeodactylum tricornutum experiments. Biomass 5:181–209

    Article  Google Scholar 

  • Tóth S, Schansker G, Strasser R (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93:193–203

  • Vårum KM, Østgaard K, Grimsrud K (1986) Diurnal rhythms in carbohydrate metabolism of the marine diatom Skeletonema costatum (Grev.) Cleve. J Exp Mar Biol Ecol 102:249–256

    Article  Google Scholar 

  • Wagner H, Jakob T, Wilhelm C (2006) Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytol 169:95–108

    Article  CAS  PubMed  Google Scholar 

  • Wagner H, Liu Z, Langner U, Stehfest K, Wilhelm C (2010) The use of FTIR spectroscopy to assess quantitative changes in the biochemical composition of microalgae. J Biophotonics 3:557–566

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm C, Jungandreas A, Jakob T, Goss R (2014) Light acclimation in diatoms: from phenomenology to mechanisms. Mar Genomics 16:5–15

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank the Deutsche Forschungsgemeinschaft (DFG) for financial support (grant numbers Wi 764/10, Wi 764/14 and Wi 764/19). J. Lavaud thanks the University of Konstanz, the DFG (grant LA 2368/2-1), and the CNRS for their financial support.

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Correspondence to Torsten Jakob.

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Wagner, H., Jakob, T., Lavaud, J. et al. Photosystem II cycle activity and alternative electron transport in the diatom Phaeodactylum tricornutum under dynamic light conditions and nitrogen limitation. Photosynth Res 128, 151–161 (2016). https://doi.org/10.1007/s11120-015-0209-7

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