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Variation of the photosynthetic electron transfer rate and electron requirement for daily net carbon fixation in Ariake Bay, Japan

Abstract

Fast repetition rate fluorometry (FRRf) provides a potential means to examine marine primary productivity; however, FRRf-based productivity estimations require knowledge of the electron requirement (K) for carbon (C) uptake (K C) to scale an electron transfer rate (ETR) to the CO2 uptake rate. Most previous studies have derived K C from parallel measurements of ETR and CO2 uptake over relatively short incubations, with few from longer-term daily-integrated periods. Here we determined K C by comparing depth-specific, daily ETRs and CO2-uptake rates obtained from 24-h on-deck incubation experiments undertaken on seven cruises in Ariake Bay, Japan, from 2008 to 2010. The purpose of this study was to determine the extent of variability of K C and to what extent this variability could be reconciled with the prevailing environmental conditions and ultimately to develop a method for determining net primary productivity (NPP) based on FRRf measurements. Both daily ETR and K C of the upper layer varied considerably, from 0.5 to 115.7 mmol e mg Chl-a −1 day−1 and 4.1–26.6 mol e (mol C)−1, respectively, throughout the entire data set. Multivariate analysis revealed a strong correlation between daily photosynthetically active radiation (PAR) and K C (r 2 = 0.94). A simple PAR-dependent relationship derived from the data set was used for generating K C, and this relationship was validated by comparing the FRRf-predicted NPP with the 13C uptake measured in 2007. These new observations demonstrate the potential application of FRRf for estimating regional NPP from ETR.

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References

  • Behrenfeld MJ, Falkowski PG (1997) Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol Oceanogr 42:1–20

    Article  Google Scholar 

  • Behrenfeld MJ, Kolber ZS (1999) Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283:840–843

    Article  Google Scholar 

  • Brading P, Warner ME, Smith DJ, Suggett DJ (2013) Contrasting modes of inorganic carbon acquisition amongst Symbiodinium (Dinophyceae) phylotypes. New Phytol 200:432–442

    Article  Google Scholar 

  • Cardol P, Forti G, Finazzi G (2011) Regulation of electron transport in microalgae. BBA-Bioenergetics 1807:912–918

    Article  Google Scholar 

  • Cheah W, McMinn A, Griffiths FB, Westwood KJ, Wright SW et al (2011) Assessing Sub-Antarctic Zone primary productivity from fast repetition rate fluorometry. Deep-Sea Res II 58:2179–2188

    Article  Google Scholar 

  • Corno G, Letelier RM, Abbott MR, Karl DM (2006) Assessing primary production variability in the north pacific subtropical gyre: a comparison of fast repetition rate fluorometry and 14C measurements. J Phycol 42:51–60

    Article  Google Scholar 

  • Davison IR (1991) Environmental effects on algal photosynthesis: temperature. J Phycol 27(2–8):1991. doi:10.1111/j0022-3646.00002.x

    Google Scholar 

  • Debes H, Gaard E, Hansen B (2008) Primary production on the Faroe shelf: temporal variability and environmental influences. J Mar Syst 74:686–697

    Article  Google Scholar 

  • Fujiki T, Hosaka T, Kimoto H, Ishimaru T, Saino T (2008) In situ observation of phytoplankton productivity by an underwater profiling buoy system: use of fast repetition rate fluorometry. Mar Ecol Prog Ser 353:81–88

    Article  Google Scholar 

  • Halsey KH, O’Malley RT, Graff JR, Milligan AJ, Behrenfeld MJ (2013) A common partitioning strategy for photosynthetic products in evolutionarily distinct phytoplankton species. New Phytol 198:1030–1038

    Article  Google Scholar 

  • Hama T, Miyazaki T, Ogawa Y, Iwakuma T, Takahashi M et al (1983) Measurement of photosynthetic production of a marine phytoplankton population using a stable 13C isotope. Mar Biol 73:31–36

    Article  Google Scholar 

  • 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):e0133275. doi:10.1371/journal.pone.0133275

    Article  Google Scholar 

  • Hirawake T, Shinmyo K, Fujiwara A, S-i Saitoh (2012) Satellite remote sensing of primary productivity in the Bering and Chukchi Seas using an absorption-based approach. ICES J Mar Sci 69:1194–1204

    Article  Google Scholar 

  • Ishizaka J, Kitaura Y, Touke Y, Sasaki H, Tanaka A et al (2006) Satellite detection of red tide in Ariake Sound, 1998–2001. J Oceanogr 62:37–45

    Article  Google Scholar 

  • Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547

    Article  Google Scholar 

  • Kameda T, Ishizaka J (2005) Size-fractionated primary production estimated by a two-phytoplankton community model applicable to ocean color remote sensing. J Oceanogr 61:663–672

    Article  Google Scholar 

  • Kishino M, Takahashi M, Okami N, Ichimura S (1985) Estimation of the spectral absorption coefficients of phytoplankton in the sea. Bull Mar Sci 37:634–642

    Google Scholar 

  • Kolber ZS, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38:1646–1665

    Article  Google Scholar 

  • Kolber ZS, Prášil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. BBA-Bioenergetics 1367:88–106

    Article  Google Scholar 

  • Kromkamp JC, Dijkman NA, Peene J, Simis SG, Gons HJ (2008) Estimating phytoplankton primary production in Lake IJsselmeer (The Netherlands) using variable fluorescence (PAM-FRRF) and C-uptake techniques. Eur J Phycol 43:327–344

    Article  Google Scholar 

  • Lavaud J, Rousseau B, Etienne AL (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J Phycol 40:130–137

    Article  Google Scholar 

  • Lawrenz E, Silsbe G, Capuzzo E, Ylöstalo P, Forster RM et al (2013) Predicting the electron requirement for carbon fixation in seas and oceans. PLoS One 8(3):e58137. doi:10.1371/journal.pone.0058137

    Article  Google Scholar 

  • López-Sandoval DC, Rodríguez-Ramos T, Cermeño P, Sobrino C, Marañón E (2014) Photosynthesis and respiration in marine phytoplankton: relationship with cell size, taxonomic affiliation, and growth phase. J Exp Mar Biol Ecol 457:151–159

    Article  Google Scholar 

  • Mackey KR, Paytan A, Grossman AR, Bailey S (2008) A photosynthetic strategy for coping in a high-light, low-nutrient environment. Limnol Oceanogr 53:900–913

    Article  Google Scholar 

  • Marra JF (2009) Net and gross productivity: weighing in with 14C. Aquat Microb Ecol 56:123–131

    Article  Google Scholar 

  • Marra JF (2015) Ocean productivity: a personal perspective since the first Liege Colloquium. J Mar Syst 147:3–8

    Article  Google Scholar 

  • McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR et al (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). BBA-Bioenergetics 1807:954–967

    Article  Google Scholar 

  • Melrose DC, Oviatt CA, O Reilly JE, Berman MS (2006) Comparisons of fast repetition rate fluorescence estimated primary production and 14C uptake by phytoplankton. Mar Ecol Prog Ser 311:37–46

    Article  Google Scholar 

  • Mino Y, Matsumura S, Lirdwitayaprasit T, Fujiki T, Yanagi T et al (2014) Variations in phytoplankton photo-physiology and productivity in a dynamic eutrophic ecosystem: a fast repetition rate fluorometer-based study. J Plankton Res 36:398–411

    Article  Google Scholar 

  • Moore CM, Suggett DJ, Hickman AE, Kim Y-N, Tweddle JF et al (2006) Phytoplankton photoacclimation and photoadaptation in response to environmental gradients in a shelf sea. Limnol Oceanogr 51:936–949

    Article  Google Scholar 

  • Moore CM, Mills MM, Langlois R, Milne A, Achterberg EP et al (2008) Relative influence of nitrogen and phosphorous availability on phytoplankton physiology and productivity in the oligotrophic sub-tropical North Atlantic Ocean. Limnol Oceanogr 53:291–305

    Article  Google Scholar 

  • Ott T, Clarke J, Birks K, Johnson G (1999) Regulation of the photosynthetic electron transport chain. Planta 209:250–258

    Article  Google Scholar 

  • Oxborough K, Moore CM, Suggett DJ, Lawson T, Chan HG et al (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: Methods 10:142–154

    Article  Google Scholar 

  • Prasil O, Kolber Z, Berry JA, Falkowski PG (1996) Cyclic electron flow around photosystem II in vivo. Photosynth Res 48:395–410

    Article  Google Scholar 

  • Raateoja M, Seppälä J, Kuosa H (2004) Bio-optical modelling of primary production in the SW Finnish coastal zone, Baltic Sea: fast repetition rate fluorometry in Case 2 waters. Mar Ecol Prog Ser 267:9–26

    Article  Google Scholar 

  • Robinson C, Suggett D, Cherukuru N, Ralph P, Doblin M (2014) Performance of fast repetition rate fluorometry based estimates of primary productivity in coastal waters. J Mar Syst 139:299–310

    Article  Google Scholar 

  • Saba VS, Friedrichs MAM, Antoine D, Armstrong RA, Asanuma I et al (2011) An evaluation of ocean color model estimates of marine primary productivity in coastal and pelagic regions across the globe. Biogeosciences 8:489–503

    Article  Google Scholar 

  • Schuback N, Schallenberg C, Duckham C, Maldonado MT, Tortell PD (2015) Interacting effects of light and iron availability on the coupling of photosynthetic electron transport and CO2-assimilation in marine phytoplankton. PLoS One 10(7):e0133235. doi:10.1371/journal.pone.0133235

    Article  Google Scholar 

  • Serôdio J, Lavaud J (2011) A model for describing the light response of the nonphotochemical quenching of chlorophyll fluorescence. Photosynth Res 108:61–76

    Article  Google Scholar 

  • Shibata T, Tripathy SC, Ishizaka J (2010) Phytoplankton pigment change as a photoadaptive response to light variation caused by tidal cycle in Ariake Bay, Japan. J Oceanogr 66:831–843

    Article  Google Scholar 

  • Silsbe GM, Oxborough K, Suggett DJ, Forster RM, Ihnken S et al (2015) Toward autonomous measurements of photosynthetic electron transport rates: an evaluation of active fluorescence-based measurements of photochemistry. Limnol Oceanogr: Methods 13:138–155

    Article  Google Scholar 

  • Smyth T, Pemberton K, Aiken J, Geider R (2004) A methodology to determine primary production and phytoplankton photosynthetic parameters from fast repetition rate fluorometry. J Plankton Res 26:1337–1350

    Article  Google Scholar 

  • Suggett DJ, Kraay G, Holligan P, Davey M, Aiken J et al (2001) Assessment of photosynthesis in a spring cyanobacterial bloom by use of a fast repetition rate fluorometer. Limnol Oceanogr 46:802–810

    Article  Google Scholar 

  • Suggett DJ, MacIntyre HL, Geider RJ (2004) Evaluation of biophysical and optical determinations of light absorption by photosystem II in phytoplankton. Limnol Oceanogr: Methods 2:316–332

    Article  Google Scholar 

  • Suggett DJ, Moore CM, Marañón E, Omachi C, Varela RA et al (2006a) Photosynthetic electron turnover in the tropical and subtropical Atlantic Ocean. Deep-Sea Res II:1573–1592

    Google Scholar 

  • Suggett DJ, Maberly SC, Geider RJ (2006b) Gross photosynthesis and lake community metabolism during the spring phytoplankton bloom. Limnol Oceanogr 51:2064–2076

    Article  Google Scholar 

  • Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S et al (2008) Photosynthesis and production of hydrogen peroxide by symbiodinium (pyrrhophyta) phylotypes with different thermal tolerances. J Phycol 44:948–956

    Article  Google Scholar 

  • Suggett DJ, MacIntyre HL, Kana TM, Geider RJ (2009a) Comparing electron transport with gas exchange: parameterising exchange rates between alternative photosynthetic currencies for eukaryotic phytoplankton. Aquat Microb Ecol 56:147–162

    Article  Google Scholar 

  • Suggett DJ, Moore CM, Hickman AE, Geider RJ (2009b) Interpretation of fast repetition rate (FRR) fluorescence: signatures of phytoplankton community structure versus physiological state. Mar Ecol Prog Ser 376:1–19

    Article  Google Scholar 

  • Suggett DJ, Moore MC, Geider RJ (2011) Estimating aquatic productivity from active fluorescence measurements. In: Chlorophyll a fluorescence in aquatic sciences: methods and applications, Chapter 6. Springer, pp 103–115

  • Suggett DJ, Goyen S, Evenhuis C, Szabó M, Pettay DT et al (2015) Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytol 208:370–381

    Article  Google Scholar 

  • Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N,N-dimethylformamide. J Oceanogr Soc Jpn 46:190–194

    Article  Google Scholar 

  • Tabata T, Hiramatsu K, Harada M (2015) Assessment of the water quality in the ariake sea using principal component analysis. J Water Resour Prot 7:41–49

    Article  Google Scholar 

  • Tripathy SC, Ishizaka J, Fujiki T, Shibata T, Okamura K et al (2010) Assessment of carbon- and fluorescence-based primary productivity in Ariake Bay, southwestern Japan. Estuar Coast Shelf Sci 87:163–173

    Article  Google Scholar 

  • Tripathy SC, Ishizaka J, Siswanto E, Shibata T, Mino Y (2012) Modification of the vertically generalized production model for the turbid waters of Ariake Bay, southwestern Japan. Estuar Coast Shelf S 97:66–77

    Article  Google Scholar 

  • Wang SQ, Ishizaka J, Yamaguchi H, Tripathy SC, Hayashi M et al (2014) Influence of the Changjiang River on the light absorption properties of phytoplankton from the East China Sea. Biogeosciences 11:1759–1773

    Article  Google Scholar 

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Acknowledgments

We wish to thank the captain, officers and crew of T/V-Kakuyo Maru for their admirable assistance during onboard sampling and measurements. We also thank Drs. W. Cheah, J.I. Goes and H. do R. Gomes and two reviewers for helping to improve this manuscript. This research was supported by the Global Observation Mission-Climate (GCOM-C) Project of the Japan Aerospace Exploration Agency. The contribution by D.J. Suggett was supported by an Australian Research Council Future Fellowship (FT130100202).

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Correspondence to J. Ishizaka.

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Zhu, Y., Ishizaka, J., Tripathy, S.C. et al. Variation of the photosynthetic electron transfer rate and electron requirement for daily net carbon fixation in Ariake Bay, Japan. J Oceanogr 72, 761–776 (2016). https://doi.org/10.1007/s10872-016-0370-4

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  • DOI: https://doi.org/10.1007/s10872-016-0370-4

Keywords

  • FRR fluorometry
  • Primary productivity
  • ETR
  • Quantum requirement for carbon fixation
  • 13C-uptake