Abstract
Cell size has implications for the package effect in photon absorption as well as for metabolic scaling of metabolism. In this study, we have avoided species-related differences by using isolates of the marine planktonic diatom Coscinodiscus granii with cells of different sizes and grown at different light intensities to investigate their energy allocation strategies. To make full use of incident light, several fold variations in cellular chlorophyll a content were employed across cell size. This modulation of pigment-related light absorbance was deemed effective as similar light absorbing capacities were found in all treatments. Unexpected low values of O2 evolution rate at the highest irradiance level of 450 μmol photons m−2 s−1 were found in medium and large cells, regardless of more photons being absorbed under these conditions, suggesting the operation of alternative electron flows acting as electron sinks. The growth rate was generally larger at higher irradiance levels except for the large cells, in which growth slowed at 450 μmol photons m−2 s−1, suggesting that larger cells achieved a balance between growth and photoprotection by sacrificing growth rate when exposed to high light. Although the ratio of carbon demand to rates of uncatalysed CO2 diffusion to the cell surface reached around 20 in large cells grown under higher irradiance, the carbon fixation rate was not lowered, due to the presence of a highly effective carbon dioxide concentrating mechanism.
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References
Agustí S (1991) Allometric scaling of light absorption and scattering by phytoplankton cells. Can J Fish Aquat Sci 48:763–767. https://doi.org/10.1139/f91-091
Anderson LG, Turner DR, Wedborg M, Dyrssen D (1999) Determination of total alkalinity and total dissolved inorganic carbon. In: Kremling K, Ehrhards M (eds) Methods of seawater analysis. Wiley, Weinheim, pp 127–148
Badger MR, Caemmerer S von, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philos Trans R Soc B 355:1433–1446. https://doi.org/10.1098/rstb.2000.0704
Beardall J, Allen D, Bragg J et al (2009) Allometry and stoichiometry of unicellular, colonial and multicellular phytoplankton. New Phytol 181:295–309. https://doi.org/10.1111/j.1469-8137.2008.02660.x
Behrenfeld MJ, Halsey KH, Milligan AJ (2008) Evolved physiological responses of phytoplankton to their integrated growth environment. Philos Trans R Soc B 363:2687–2703. https://doi.org/10.1098/rstb.2008.0019
Bidigare RR, Ondrusek ME, Morrow JH, Kiefer DA (1990) In-vivo absorption properties of algal pigments. Proc SPIE Ocean Optics X 1302:290–303. https://doi.org/10.1117/12.21451
Burkhardt S, Zondervan I, Riebesell U (1999) Effect of CO2 concentration on C:N:P ratio in marine phytoplankton: a species comparison. Limnol Oceanogr 44(3):683–690. https://doi.org/10.4319/lo.1999.44.3.0683
Cleveland JS, Weidemann AD (1993) Quantifying absorption by aquatic particles: a multiple scattering correction for glass-fiber filters. Limnol Oceanogr 38:1321–1327. https://doi.org/10.4319/lo.1993.38.6.1321
Cruz S, Goss R, Wilhelm C et al (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. https://doi.org/10.1093/jxb/erq284
Culver ME, Perry MJ (1999) The response of photosynthetic absorption coefficients to irradiance in culture and in tidally mixed estuarine waters. Limnol Oceanogr 44:24–36. https://doi.org/10.4319/lo.1999.44.1.0024
Curien G, Flori S, Villanova V et al (2016) The water to water cycles in microalgae. Plant Cell Physiol 57:1354–1363. https://doi.org/10.1093/pcp/pcw048
Domingues N, Matos AR, Marques da Silva J, Cartaxana P (2012) Response of the diatom Phaeodactylum tricornutum to photooxidative stress resulting from high light exposure. PLoS ONE 7:e38162. https://doi.org/10.1371/journal.pone.0038162
Dubinsky Z, Stambler N (2009) Photoacclimation processes in phytoplankton: mechanisms, consequences, and applications. Aquat Microb Ecol 56:163–176. https://doi.org/10.3354/ame01345
Falkowski PG, Owens TG, Ley AC, Mauzerall DC (1981) Effects of growth irradiance levels on the ratio of reaction centers in two species of marine phytoplankton. Plant Physiol 68:969–973
Finkel ZV, Irwin AJ, Schofield O (2004) Resource limitation alters the ¾ size scaling of metabolic rates in phytoplankton. Mar Ecol Prog Ser 273:269–280
Finkel ZV, Beardall J, Flynn KJ et al (2010) Phytoplankton in a changing world: cell size and elemental stoichiometry. J Plankton Res 32:119–137. https://doi.org/10.1093/plankt/fbp098
Fisher NL, Halsey KH (2016) Mechanisms that increase the growth efficiency of diatoms in low light. Photosynth Res 129:183–197. https://doi.org/10.1007/s11120-016-0282-6
Flynn KJ, Blackford JC, Baird ME et al (2012) Changes in pH at the exterior surface of plankton with ocean acidification. Nat Clim Change 2:510–513. https://doi.org/10.1038/nclimate1489
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 24:859–874. https://doi.org/10.1093/plankt/24.9.859
Fukao T, Kimoto K, Yamatogi T et al (2009) Marine mucilage in Ariake Sound, Japan, is composed of transparent exopolymer particles produced by the diatom Coscinodiscus granii. Fish Sci 75:1007–1014. https://doi.org/10.1007/s12562-009-0122-0
Gilbert M, Domin A, Becker A, Wilhelm C (2000a) Estimation of primary productivity by Chlorophyll a in vivo fluorescence in freshwater phytoplankton. Photosynth 38:111–126. https://doi.org/10.1023/A:1026708327185
Gilbert M, Wilhelm C, Richter M (2000b) 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. https://doi.org/10.1016/S0176-1617(00)80052-8
Goldman JC (1999) Inorganic carbon availability and the growth of large marine diatoms. Mar Ecol Prog Ser 180:81–91. https://doi.org/10.3354/meps180081
Goss R, Jakob T (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth Res 106:103–122. https://doi.org/10.1007/s11120-010-9536-x
Helbling EW, Chalker BE, Dunlap WC et al (1996) Photoacclimation of Antarctic marine diatoms to solar ultraviolet radiation. J Exp Mar Biol Ecol 204:85–101. https://doi.org/10.1016/0022-0981(96)02591-9
Jakob T, Schreiber U, Kirchesch V et al (2005) Estimation of chlorophyll content and daily primary production of the major algal groups by means of multiwavelength-excitation PAM chlorophyll fluorometry: performance and methodological limits. Photosynth Res 83(3):343–361. https://doi.org/10.1007/s11120-005-1329-2
Key T, McCarthy A, Campbell DA et al (2010) Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environ Microbiol 12:95–104. https://doi.org/10.1111/j.1462-2920.2009.02046.x
Klughammer C, Schreiber U (2008) Saturation pulse method for assessment of energy conversion in PS I. PAM Appl Notes 1:11–14
Kraberg A, Marcus B, Claus-Dieter D (2010) Coastal phytoplankton: photo guide for Northern European Seas. Pfeil, Munich
Kühn SF, Köhler-Rink S (2008) pH effect on the susceptibility to parasitoid infection in the marine diatom Coscinodiscus spp. (Bacillariophyceae). Mar Biol 154:109–116. https://doi.org/10.1007/s00227-008-0904-4
Kühn SF, Raven JA (2007) Photosynthetic oscillation in individual cells of the marine diatom Coscinodiscus wailesii (Bacillariophyceae) revealed by microsensor measurements. Photosynth Res 95:37–44. https://doi.org/10.1007/s11120-007-9221-x
Lavaud J (2002) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol 129:1398–1406. https://doi.org/10.1104/pp.002014
Lewis E, Wallace D, Allison LJ (1998) Program developed for CO2 system calculations. In: Ocean CO2. http://cdiac.ornl.gov/oceans/co2rprt.html
Li G, Talmy D, Campbell DA (2017) Diatom growth responses to photoperiod and light are predictable from diel reductant generation. J Phycol 53:95–107. https://doi.org/10.1111/jpy.12483
Litchman E, Klausmeier CA, Schofield OM, Falkowski PG (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett 10:1170–1181. https://doi.org/10.1111/j.1461-0248.2007.01117.x
Mitchell GB, Kiefer DA (1988a) Chlorophyll a specific absorption and fluorescence excitation spectra for light-limited phytoplankton. Deep Sea Res A 35:639–663. https://doi.org/10.1016/0198-0149(88)90024-6
Mitchell GB, Kieper DA (1988b) Variability in pigment particulate fluorescence and absorption spectra in the northeastern Pacific Ocean. Deep Sea Res A 35:665–689. https://doi.org/10.1016/0198-0149(88)90025-8
Miyake C (2010) Alternative electron flows (water–water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol 51:1951–1963. https://doi.org/10.1093/pcp/pcq173
Moisan TA, Mitchell BG (1999) Photophysiological acclimation of Phaeocystis antarctica Karsten under light limitation. Limnol Oceanogr 44:247–258. https://doi.org/10.4319/lo.1999.44.2.0247
Morel A, Bricaud A (1981) Theoretical results concerning light absorption in a discrete medium, and application to specific absorption of phytoplankton. Deep Sea Res A 28:1375–1393. https://doi.org/10.1016/0198-0149(81)90039-X
Morel FMM, Rueter JG, Anderson DM, Guillard RRL (1979) Aquil: a chemically defined phytoplankton culture medium for trace metal studies. J Phycol 15:135–141. https://doi.org/10.1111/j.1529-8817.1979.tb02976.x
Mueller B, den Haan J, Visser PM et al (2016) Effect of light and nutrient availability on the release of dissolved organic carbon (DOC) by Caribbean turf algae. Sci Rep 6:23248. https://doi.org/10.1038/srep23248
Nagai S, Hori Y, Manabe T, Imai I (1995) Restoration of cell size by vegetative cell enlargement in Coscinodiscus wailesii (Bacillariophyceae). Phycologia 34:533–535. https://doi.org/10.2216/i0031-8884-34-6-533.1
Nobel PS (1999) Physicochemical & environmental plant physiology. Academic Press, San Diego
Ploug H, Stolte W, Epping EHG (1999) Diffusive boundary layers, photosynthesis, and respiration of the colony-forming plankton alga. Phaeocystis sp. Limnol Oceanogr 44:1949–1958. https://doi.org/10.4319/lo.1999.44.8.1949
Qiao H, Fan X, Xu D et al (2015) Artificial leaf aids analysis of chlorophyll fluorescence and P700 absorbance in studies involving microalgae. Phycol Res 63:72–76. https://doi.org/10.1111/pre.12073
Ritchie RJ (2006) Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res 89:27–41. https://doi.org/10.1007/s11120-006-9065-9
Roselli L, Stanca E, Paparella F et al (2013) Determination of Coscinodiscus cf. granii biovolume by confocal microscopy: comparison of calculation models. J Plankton Res 35:135–145. https://doi.org/10.1093/plankt/fbs069
Sharpe SC, Koester JA, Loebl M et al (2012) Influence of cell size and DNA content on growth rate and photosystem II Function in cryptic species of Ditylum brightwellii. PLOS ONE 7:e52916. https://doi.org/10.1371/journal.pone.0052916
Shikanai T (2014) Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr Opin Biotechnol 26:25–30. https://doi.org/10.1016/j.copbio.2013.08.012
Stein JR (1979) Handbook of phycological methods: culture methods and growth measurements. Cambridge University Press, Cambridge
Stuart V, Sathyendranath S, Platt T et al (1998) Pigments and species composition of natural phytoplankton populations: effect on the absorption spectra. J Plankton Res 20:187–217. https://doi.org/10.1093/plankt/20.2.187
Taylor NJ (1985) Silica incorporation in the diatom Coscinodiscus granii as affected by light intensity. Br Phycol J 20:365–374. https://doi.org/10.1080/00071618500650371
Thingstad TF, Øvreås L, Egge JK et al (2005) Use of non-limiting substrates to increase size; a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs? Ecol Lett 8:675–682. https://doi.org/10.1111/j.1461-0248.2005.00768.x
Von Stosch HA (1981) Structural and histochemical observations on the organic layers of the diatom cell wall. In: Proceedings of the 6th Diatom Symposium on Recent and Fossil Diatoms. Otto Koetz, Science Publishers, Königstein, pp 231–252
Vredenberg WJ, Bulychev AA (2010) Photoelectrochemical control of the balance between cyclic- and linear electron transport in photosystem I. Algorithm for P700 + induction kinetics. Biochim Biophys Acta BBA 1797:1521–1532. https://doi.org/10.1016/j.bbabio.2010.03.019
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. https://doi.org/10.1111/j.1469-8137.2005.01550.x
Wagner H, Jakob T, Lavaud J, Wilhelm C (2016) 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. https://doi.org/10.1007/s11120-015-0209-7
Wagner H, Jakob T, Fanesi A, Wilhelm C (2017) Towards an understanding of the molecular regulation of carbon allocation in diatoms: the interaction of energy and carbon allocation. Phil Trans R Soc B 372:20160410. https://doi.org/10.1098/rstb.2016.041
Wientjes E, van Amerongen H, Croce R (2013) LHCII is an antenna of both photosystems after long-term acclimation. Biochim Biophys Acta BBA 1827:420–426. https://doi.org/10.1016/j.bbabio.2012.12.009
Wilhelm C, Jungandreas A, Jakob T, Goss R (2014) Light acclimation in diatoms: from phenomenology to mechanisms. Mar Diatoms 16:5–15. https://doi.org/10.1016/j.margen.2013.12.003
Wolf-Gladrow D, Riebesell U (1997) Diffusion and reactions in the vicinity of plankton: a refined model for inorganic carbon transport. Mar Chem 59:17–34. https://doi.org/10.1016/S0304-4203(97)00069-8
Wu Y, Campbell DA, Irwin AJ et al (2014) Ocean acidification enhances the growth rate of larger diatoms. Limnol Oceanogr 59:1027–1034. https://doi.org/10.4319/lo.2014.59.3.1027
Acknowledgements
The authors would like to thank the two anonymous reviewers for their helpful comments. This study was supported by National Natural Science Foundation (41430967, 41720104005, 41721005), a joint project of National Natural Science Foundation of China and Shandong Province (No. U1606404).
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Yan, D., Beardall, J. & Gao, K. Variation in cell size of the diatom Coscinodiscus granii influences photosynthetic performance and growth. Photosynth Res 137, 41–52 (2018). https://doi.org/10.1007/s11120-017-0476-6
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DOI: https://doi.org/10.1007/s11120-017-0476-6