Abstract
Diatoms account for about 40% of primary production in highly productive ecosystems. The development of a new generation of fluorometers has made it possible to improve estimation of the electron transport rate from photosystem II, which, when coupled with the carbon incorporation rate enables estimation of the electrons required for carbon fixation. The aim of this study was to investigate the daily dynamics of these electron requirements as a function of the diel light cycle in three relevant diatom species and to apprehend if the method of estimating the electron transport rate can lead to different pictures of the dynamics. The results confirmed the species-dependent capacity for photoacclimation under increasing light levels. Despite daily variations in the photosynthetic parameters, the results of this study underline the low daily variability of the electron requirements estimated using functional absorption of the photosystem II compared to an estimation based on a specific absorption cross section of chlorophyll a. The stability of the electron requirements throughout the day would suggest it is potentially possible to estimate high-frequency primary production by using autonomous variable fluorescence measurements from ships-of-opportunity or moorings, without taking potential daily variation in this parameter into consideration, but this result has to be confirmed on natural phytoplankton assemblages. The results obtained in this study confirm the low electron requirements of diatoms to perform photosynthesis, and suggest a potential additional source of energy for carbon fixation, as recently described in the literature for this class.
Similar content being viewed by others
References
Armbrust EV (2009) The life of diatoms in the world’s oceans. Nature 459(7244):185–192
Babin M, Morel A, Gagnon R (1994) An incubator designed for extensive and sensitive measurements phytoplankton photosynthetic parameters. Limnol Oceanogr 39(3):694–702
Babin M, Morel A, Claustre H, Bricaud A, Kolber Z, Falkowski PG (1996) Nitrogen- and irradiance-dependent variations of the maximum quantum yield of carbon fixation in eutrophic, mesotrophic and oligotrophic marine systems. Deep Sea Res 43(8):1241–1272
Bailleul B, Berne N, Murik O, Petroutsos D, Prihoda J, Tanaka A et al (2015) Mitochondria drives CO2 assimilation in diatoms. Nature 524:366–369
Barranguet C, Kromkamp J (2000) Estimating primary production rates from photosynthetic electron transport in estuarine microphytobenthos. Mar Ecol Prog Ser 204:39–52
Behrenfeld MJ, Prasil O, Babin M, Bruyant F (2004) in Search of a physiological basis for covariations in light-limited and light-saturated photosynthesis. J Phycol 40(1):4–25
Buesseler KO (1998) The decoupling of production and particulate export in the surface ocean. Glob Biogeochem Cycles 12(2):297–310
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(1):33–41
Claquin P, Probert I, Lefebvre S, Veron B (2008) Effects of temperature on photosynthetic parameters and TEP production in eight species of marine microalgae. Aquat Microb Ecol 51(1):1–11
Cloern JE, Foster SQ, Kleckner a E (2014) Phytoplankton primary production in the world’s estuarine-coastal ecosystems. Biogeosciences 11(9):2477–2501
Dimier C, Corato F, Tramontano F, Brunet C (2007) Photoprotection and xanthophyll-cycle activity in three marine diatoms. J Phycol 43(5):937–947
Dimier C, Giovanni S, Ferdinando T, Brunet C (2009) Comparative ecophysiology of the xanthophyll cycle in six marine phytoplanktonic species. Protist 160(3):397–411
Dubinsky Z, Stambler N (2009) Photoacclimation processes in phytoplankton: mechanisms, consequences, and applications. Aquat Microb Ecol 56(2–3):163–176
Dubinsky Z, Falkowski PG, Wyman K (1986) Light harvesting and utilization by phytoplankton. Plant Cell Physiol 27(7):1335–1349
Ducklow HW, Steinberg DK, Buesseler KO (2001) Upper ocean carbon export and the biological pump. Oceanography 14(4):50–58
Eilers PHC, Peeters JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Model 42(3–4):199–215
Falkowski PG (1984) Physiological responses of phytoplankton to natural light regimes. 6(2):295–307
Fujiki T, Taguchi S (2002) Variability in chlorophyll a specific absorption coefficient in marine phytoplankton as a function of cell size and irradiance. J Plankton Res 24(9):859–874
Geider RJ, Delucia EH, Falkowski PG, Finzi AC, Grime JP, Grace J et al. (2001) Primary productivity of planet earth: biological determinants and physical constraints in terrestrial and aquatic habitats. Glob Change Biol 7(8):849–882
Gilbert M, Wilhelm C, Richter M (2000) Bio-optical modelling of oxygen evolution using in vivo fluorescence: comparison of measured and calculated photosynthesis/irradiance (P-I) curves in four representative phytoplankton species. J Plant Physiol 157(3):307–314. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0176161700800528
Greene RM, Kolber ZS, Swift DG, Tindale NW, Falkowski PG (1994) Physiological limitation of phytoplankton photosynthesis in the eastern equatorial pacific determined from variability in the quantum yield of fluorescence. Limnol Oceanogr 39(5):1061–1074
Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8(2):229–239
Hama T, Miyazaki T, Ogawa Y, Iwakuma T, Takahashi M, Otsuki A et al (1983) Measurement of photosynthetic production of a marine phytoplankton population using a stable 13C isotope. Mar Biol 73:31–36
Hancke K, Hancke TB, Lasse M, Olsen LM, Johnsen G, Ronnie N (2008a) Temperature effects on microalgal photosynthesis-light responses measured by O2 production, pulse-amplitude-modulated fluorescence, and 14C assimilation. J Phycol 44:501–514
Hancke K, Hancke TB, Olsen LM, Johnsen G, Glud RN (2008b) Temperature effects on microalgal photosynthesis-light responses measured by O2 production, pulse-amplitued-modelated fluorescence and 14C assimilation. 514:501–514
Hancke K, Dalsgaard T, Sejr MK, Markager S, Glud RN (2015) Phytoplankton productivity in an arctic fjord (West Greenland): estimating electron requirements for carbon fixation and oxygen production. PLoS ONE 10(7):1–23
Henson SA, Sanders R, Madsen E (2012) Global patterns in efficiency of particulate organic carbon export and transfer to the deep ocean. Global Biogeochem Cycles 26(1):1–14
Houliez E, Simis S, Nenonen S, Ylöstalo P, Seppälä J (2017) Basin-scale spatio-temporal variability and control of phytoplankton photosynthesis in the Baltic Sea: the first multiwavelength fast repetition rate fluorescence study operated on a ship-of-opportunity. J Mar Syst 169:40–51
Huisman J, Sharples J, Stroom JM, Visser PM, Kardinaal WEA, Verspagen J et al. (2004) Changes in turbulent mixing shift competition for light between phytoplakton species. 85(11):2960–2970
Johnsen G, Sakshaug E (2007) Biooptical characteristics of PSII and PSI in 33 species (13 pigment groups) of marine phytoplankton, and the relevance for pulse-amplitude-modulated and fast-repetition-rate fluorometry 1. J Phycol 43(6):1236–1251
Jouenne F, Lefebvre S, Véron B, Lagadeuc Y (2005) Biological and physicochemical factors controlling short-term variability in phytoplankton primary production and photosynthetic parameters in a macrotidal ecosystem (eastern English Channel). Estuar Coast Shelf Sci 65(3):421–439
Juneau P, Harrison PJ (2005) Comparison by PAM fluorometry of photosynthetic activity of nine marine phytoplankton grown under identical conditions. Photochem Photobiol 81(3):649–653
Kaiblinger C, Dokulil MT (2006) Application of fast repetition rate fluorometry to phytoplankton photosynthetic parameters in freshwaters. Photosynth Res 88(1):19–30
Key T, McCarthy A, Campbell DA, Six C, Roy S, Finkel ZV (2010) Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environ Microbiol 12(1):95–104
Kolber Z, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38(8):1646–1665
Kromkamp JC, Forster RM (2003) The use of variable fluorescence measurements in aquatic ecosystems: differences between multiple and single turnover measuring protocols and suggested terminology. Eur J Phycol 38:103–112
Lavaud J (2007) Fast regulation of photosynthesis in diatoms: mechanisms, evolution and ecophysiology [Internet]. Vol. 1, Funct Plant Sci Biotechonol. Available from: https://hal.archives-ouvertes.fr/hal-01094678/
Lavaud J, Strzepek RF, Kroth PG (2007) Photoprotection capacity differs among diatoms: possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnol Oceanogr 52(3):1188–1194
Lavergne J, Trissl HW (1995) Theory of fluorescence induction in photosystem II: derivation of analytical expressions in a model including exciton-radical-pair equilibrium and restricted energy transfer between photosynthetic units. Biophys J 68(6):2474–2492
Lawrenz E, Silsbe G, Capuzzo E, Ylöstalo P, Forster RM, Simis SGH et al (2013) Predicting the electron requirement for carbon fixation in seas and oceans. PLoS One 8(3):e58137
Litchman E (1998) Population and community responses of phytoplankton to fluctuating light. Oecologia 117:247–257
MacIntyre H, Cullen J (1996) Primary production by suspended and benthic microalgae in a turbid estuary:time-scales of variability in San Antonio Bay, Texas. Mar Ecol Prog Ser 145(1–3):245–268
Macintyre HL, Kana TM, Anning T, Geider RJ (2002) Review photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38
Marchetti A, Juneau P, Whitney FA, Wong CS, Harrison PJ (2006) Phytoplankton processes during a mesoscale iron enrichment in the NE subarctic Pacific: part II-Nutrient utilization. Deep Sea Res Part II 53(20–22):2114–2130
Martin-Jézéquel V, Hildebrand M, Brzezinski MA (2000) Silicon metabolism in diatoms: implications for growth. J Phycol 36(5):821–840. https://doi.org/10.1046/j.1529-8817.2000.00019.x
Morris EP, Kromkamp JC (2003 May) Influence of temperature on the relationship between oxygen- and fluorescence-based estimates of photosynthetic parameters in a marine benthic diatom (Cylindrotheca closterium). Eur J Phycol 38(2):133–142
Napoléon C, Claquin P (2012) Multi-parametric relationships between PAM measurements and carbon incorporation, an in situ approach. PLoS ONE 7(7):1–12
Napoléon C, Fiant L, Raimbault V, Claquin P (2013a) Study of dynamics of phytoplankton and photosynthetic parameters using opportunity ships in the western English Channel. J Mar Syst 128:146–158
Napoléon C, Raimbault V, Claquin P (2013b) Influence of Nutrient Stress on the relationships between PAM measurements and carbon incorporation in four phytoplankton species. PLoS ONE 8(6):e66423
Nelson DM, Tréguer P, Brzezinski MA, Leynaert A, Quéguiner B (1995) Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob Biogeochem Cycle 9:359–372
Oxborough K, Moore CM, Suggett DJ, Lawson T, Chan HG, Geider RJ (2012) Direct estimation of functional PSII reaction center concentration and PSII electron flux on a volume basis: a new approach to the analysis of Fast Repetition Rate fluorometry (FRRf) data. Limnol Oceanogr 10:142–154
Pauly D, Christensen V (1995) Primary production required to sustain global fisheries. 374(March):255–257
Prézelin BB (1992) Diel periodicity in phytoplankton productivity. Hydrobiologia 238(1):1–35
Schreiber U, Klughammer C, Kolbowski J (2012) Assessment of wavelength-dependent parameters of photosynthetic electron transport with a new type of multi-color PAM chlorophyll fluorometer. Photosynth Res 113(1–3):127–144
Schuback N, Hoppe CJM, Tremblay J-É, Maldonado MT, Tortell PD (2017) Primary productivity and the coupling of photosynthetic electron transport and carbon fixation in the Arctic Ocean. Limnol Oceanogr 62(3):898–921
Shibata K, Benson AA, Calvin M (1954) The absorption spectra of suspensions of living micro-organisms. Biochim et Biophysica Acta 15:461–470
Silsbe GM, Oxborough K, Suggett DJ, Forster RM, Ihnken S, Komárek O et al (2015) Toward autonomous measurements of photosynthetic electron transport rates: an evaluation of active fluorescence-based measurements of photochemistry. Limnol Oceanogr 13(3):138–155
Suggett DJ, MacIntyre HL, Geider RJ (2004) Evaluation of biophysical and optical determinations of light absorption by photosystem II in phytoplankton. Limnol Oceanogr 2:316–332
Thorel M, Fauchot J, Morelle J, Raimbault V, Le Roy B, Miossec C et al (2014) Interactive effects of irradiance and temperature on growth and domoic acid production of the toxic diatom Pseudo-nitzschia australis (Bacillariophyceae). Harmful Algae 39:232–241
Van De Poll WH, Janknegt PJ, Van Leeuwe MA, Visser RJW, Buma AGJ (2009) Excessive irradiance and antioxidant responses of an Antarctic marine diatom exposed to iron limitation and to dynamic irradiance. J Photochem Photobiol B 94(1):32–37
Weis E, Berry JA (1987) Quantum efficiency of photosystem {II} in relation to “energy”-dependent quenching of chlorophyll fluorescence. Biochim et Biophysica Acta 894(2):198–208
Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39(8):1985–1992
Wu H, Roy S, Alami M, Green BR, Campbell DA (2012) Photosystem II photoinactivation, repair, and protection in marine centric diatoms. Plant Physiol 160(1):464–476
Zhu Y, Ishizaka J, Tripathy SC, Wang S, Mino Y, Matsuno T et al (2016) Variation of the photosynthetic electron transfer rate and electron requirement for daily net carbon fixation in Ariake Bay, Japan. J Oceanogr 72(5):761–776
Acknowledgements
We thank Juliette Fauchot and Bertrand Le Roy for providing the diatom strains and Anne-Flore Deton for technical assistance. We are also really grateful to Camille Napoleon for technical help and constructive exchanges during this study. This work was support by the GIP Seine-Aval project “PROUESSE” and the SMILE 2 project supported by l’Agence de l’Eau Seine Normandie.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Morelle, J., Claquin, P. Electron requirements for carbon incorporation along a diel light cycle in three marine diatom species. Photosynth Res 137, 201–214 (2018). https://doi.org/10.1007/s11120-018-0491-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-018-0491-2