Skip to main content
SpringerLink
Log in

Changes in the Rubisco to photosystem ratio dominates photoacclimation across phytoplankton taxa

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

When growth irradiance changes, phytoplankton acclimates by changing allocations to cellular components to re-balance their capacity to absorb photons versus their capacity to use the electrons from the oxidation of water at photosystem II. Published changes in the cellular allocations resulting from photoacclimation across algal groups highlight that algae adopt different strategies. We examined the photoacclimation of the photosynthetic apparatus of six marine phytoplankters under near-natural diel irradiance patterns. For most of the phytoplankters, Chl a per structural photosystem II unit decreased with increasing growth irradiance, but a parallel decline in optical packaging effect allowed cells to maintain their functional absorption cross section serving active photosystem II units (σ PSII). Furthermore, no significant changes were observed in the ratio of Chl a per photosystem I. The diatom Skeletonema marinoi proved an exception to this pattern as Chl a per photosystem II is stable and Chl a per photosystem I slightly decreased with light intensity. A clear decrease in the photosystem content per cell was observed for all species except for Thalassiosira oceanica and S. marinoi. Rubisco content per cell showed little variation with irradiance for most algae, except for a 3-fold increase in S. marinoi. A ~700 % increase in the Rubisco:photosystem ratio across species with increasing growth irradiance indicates this is a key cellular stoichiometric adjustment to balance photon absorption capacity and the carbon reduction capacity. Increasing the Rubisco:photosystem ratio occurs through a decrease in the photosystems per cell for most of the phytoplankters in this study, except in the case of S. marinoi where Rubisco per cell increased.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Anning T, MacIntyre HL, Pratt SM, Sammes PJ, Gibb S, Geider RJ (2000) Photoacclimation in the marine diatom Skeletonema costatum. Limnol Oceanogr 45:1807–1817

    Article  Google Scholar 

  • Babin M, Morel A, Gentili B (1996) Remote sensing of sea surface sun-induced chlorophyll fluorescence: consequences of natural variations in the optical characteristics of phytoplankton and the quantum yield of chlorophyll a fluorescence. Int J Remote Sens 17:2417–2448

    Article  Google Scholar 

  • Behrenfeld MJ, Prasil O, Kolber ZS, Babin M, Falkowski PG (1998) Compensatory changes in photosystem II electron turnover rates protect photosynthesis from photoinhibition. Photosynth Res 58:259–268

    Article  CAS  Google Scholar 

  • Bidigare RR, Ondrusek ME, Morrow JH, Kiefer DA (1990) In-vivo absorption properties of algal pigments. In: Orlando’90, 16–20 April, pp 290–302

  • Bouman HA, Ulloa O, Scanlan DJ, Zwirglmaier K, Li WKW, Platt T, Stuart V, Barlow R, Leth O, Clementson L, Lutz V, Fukasawa M, Watanabe S, Sathyendranath S (2006) Oceanographic basis of the global surface distribution of prochlorococcus ecotypes. Science 312:918–921

    Article  CAS  PubMed  Google Scholar 

  • Brand LE, Guillard RRL, Murphy LS (1981) A method for the rapid and precise determination of acclimated phytoplankton reproduction rates. J Plankton Res 3:193–201

    Article  Google Scholar 

  • Bricaud A, Claustre H, Ras J, Oubelkheir K (2004) Natural variability of phytoplanktonic absorption in oceanic waters: influence of the size structure of algal populations. J Geophys Res C 109:C110101–C1101012

    Google Scholar 

  • Brown CM, MacKinnon JD, Cockshutt AM, Villareal TA, Campbell DA (2008) Flux capacities and acclimation costs in trichodesmium from the gulf of mexico. Mar Biol 154:413–422

    Article  Google Scholar 

  • Cullen JJ, Franks PJS, Karl DM, Longhurst A (2002) Physical influences on marine ecosystem dynamics. In: Robinson AR, McCarthy JJ, Rothschild BJ (eds) The sea, vol 12. Wiley, Hoboken, pp 297–335

    Google Scholar 

  • Demmig-Adams B, Adams WW III (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26

    Article  Google Scholar 

  • Denman KL, Gargett AE (1983) Time and space scales of vertical mixing and advection of phytoplankton in the upper ocean. Limnol Oceanogr 28:801–815

    Article  Google Scholar 

  • Dubinsky Z, Schofield O (2010) From the light to the darkness: thriving at the light extremes in the oceans. Hydrobiologia 639:153–171

    Article  CAS  Google Scholar 

  • Dubinsky Z, Stambler N (2009) Photoacclimation processes in phytoplankton: mechanisms, consequences, and applications. Aquat Microb Ecol 56:163–176

    Article  Google Scholar 

  • Dubinsky Z, Falkowski PG, Wyman K (1986) Light harvesting and utilization by phytoplankton. Plant Cell Physiol 27:1335–1349

    CAS  Google Scholar 

  • Edelman M, Mattoo AK (2008) D1-protein dynamics in photosystem II: the lingering enigma. Photosynth Res 98:609–620

    Article  CAS  PubMed  Google Scholar 

  • Falkowski PG, LaRoche J (1991) Acclimation to spectral irradiance in algae. J Phycol 27:8–14

    Article  Google Scholar 

  • Falkowski PG, Owens TG (1980) Light— shade adaptation: two strategies in marine phytoplankton. Plant Physiol 66:592–595

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Falkowski PG, Raven JA (2007) Aquatic photosynthesis. Princeton University Press, Princeton

    Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fisher T, Shurtz-Swirski R, Gepstein S, Dubinsky Z (1989) Changes in the levels of ribulose-l,5-bisphosphate carboxylase/oxygenase (Rubisco) in Tetraedron minimum (Chlorophyta) during light and shade adaptation. Plant Cell Physiol 30:221–222

    CAS  Google Scholar 

  • Fisher T, Minnaard J, Dubinsky Z (1996) Photoacclimation in the marine alga Nannochloropsis sp. (Eustigmatophyte): a kinetic study. J Plankton Res 18:1797–1818

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gaffron H, Wohl K (1936) Zur theorie der assimilation. Naturwissenschaften 24:81–90

    Article  CAS  Google Scholar 

  • Geider RJ, Roche J, Greene RM, Olaizola M (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (bacillariophyceae) to nitrate, phosphate or iron starvation. J Phycol 29:755–766

    Article  CAS  Google Scholar 

  • Guillard RRL, Hargraves PE (1993) Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234–236

    Article  Google Scholar 

  • Herzig R, Dubinsky Z (1993) Effect of photoacclimation on the energy partitioning between cyclic and non-cyclic photophosphorylation. New Phytol 123:665–672

    Article  CAS  Google Scholar 

  • Hideg E, Spetea C, Vass I (1994) Singlet oxygen and free radical production during acceptor-and donor-side-induced photoinhibition: Studies with spin trapping EPR spectroscopy. Biochim Biophys Acta (BBA) 1186:143–152

    Article  CAS  Google Scholar 

  • Hideg E, Kálai T, Hideg K, Vass I (1998) Photoinhibition of photosynthesis in vivo results in singlet oxygen production detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 37:11405–11411

    Article  CAS  PubMed  Google Scholar 

  • Hobson LA, Morris WJ, Guest KP (1985) Varying photoperiod, ribulose 1, 5-bisphosphate carboxylase/oxygenase and CO2 uptake in Thalassiosira fluviatilis (bacillariophyceae). Plant Physiol 79:833–837

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hooker SB, Van Heukelem L, Thomas CS, Claustre H, Ras J, Barlow R, Sessions H, Schlüter L, Perl J, Trees C, Stuart V, Head E, Clementson L, Fishwick J, Llewellyn C, Aiken J (2005) The second SeaWiFS HPLC analysis round-robin experiment (SeaHARRE-2). NASA/TM-2005-212785. National Aeronautics and Space Administration, Goddard Space Flight Center

  • Huisman J, Sharples J, Stroom JM, Visser PM, Kardinaal WEA, Verspagen JM, Sommeijer B (2004) Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85:2960–2970

    Article  Google Scholar 

  • Huner N, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230

    Article  Google Scholar 

  • Huot Y, Babin M (2011) Overview of fluorescence protocols: theory, basic concepts, and practice. Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Netherlands, pp 31–74

    Google Scholar 

  • Iglesias-Prieto R, Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser 113:163–175

    Article  Google Scholar 

  • Kolber Z, Zehr J, Falkowski P (1988) Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Plant Physiol 88:923–929

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  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, Rousseau B, Etienne A-L (2004) General features of photoprotection by energy dissipation in planktonic diatoms (bacillariophyceae). J Phycol 40:130–137

    Article  Google Scholar 

  • 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 52:1188–1194

    Article  CAS  Google Scholar 

  • Losh JL, Young JN, Morel FM (2013) Rubisco is a small fraction of total protein in marine phytoplankton. New Phytol 198:52–58

    Article  CAS  PubMed  Google Scholar 

  • MacIntyre HL, Cullen JJ (2005) Using cultures to investigate the physiological ecology of microalgae. In: Algal culturing techniques. Elsevier Academic Press, New York, pp 287–326

  • MacIntyre HL, Kana TM, Geider RJ (2000) The effect of water motion on short-term rates of photosynthesis by marine phytoplankton. Trends Plant Sci 5:12–17

    Article  CAS  PubMed  Google Scholar 

  • MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38

    Article  Google Scholar 

  • McKew BA, Davey P, Finch SJ, Hopkins J, Lefebvre SC, Metodiev MV, Oxborough K, Raines CA, Lawson T, Geider RJ (2013a) The trade-off between the light-harvesting and photoprotective functions of fucoxanthin-chlorophyll proteins dominates light acclimation in emiliania huxleyi (clone CCMP 1516). New Phytol 200:74–85

    Article  CAS  PubMed  Google Scholar 

  • McKew BA, Lefebvre SC, Achterberg EP, Metodieva G, Raines CA, Metodiev MV, Geider RJ (2013b) Plasticity in the proteome of Emiliania huxleyi CCMP 1516 to extremes of light is highly targeted. New Phytol 200:61–73

    Article  CAS  PubMed  Google Scholar 

  • Morel A (1978) Available, usable, and stored radiant energy in relation to marine photosynthesis. Deep Sea Res 25:673–688

    Article  CAS  Google Scholar 

  • Morel A, Bricaud A (1981) Theoretical results concerning light absorption in a discrete medium, and application to specific absorption of phytoplankton. Deep Sea Res Part A 28:1375–1393

    Article  Google Scholar 

  • Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed Central  PubMed  Google Scholar 

  • Nedbal L, Trtilek M, Kaftan D (1999) Flash fluorescence induction: a novel method to study regulation of photosystem II. J Photochem Photobiol B 48:154–157

    Article  CAS  Google Scholar 

  • Oxborough K, Baker NR (2000) An evaluation of the potential triggers of photoinactivation of photosystem II in the context of a stern-volmer model for downregulation and the reversible radical pair equilibrium model. Philos Trans R Soc Lond Ser B Biol Sci 355:1489–1498

    Article  CAS  Google Scholar 

  • Parkhill J-P, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37:517–529

    Article  Google Scholar 

  • Perry MJ, Talbot MC, Alberte RS (1981) Photoadaption in marine phytoplankton: response of the photosynthetic unit. Mar Biol 62:91–101

    Article  CAS  Google Scholar 

  • Prezelin BB (1981) Light reactions in photosynthesis. Can Bull Fish Aquat Sci 210:1–43

    Google Scholar 

  • Prezelin BB, Tilzer MM, Schofield O, Haese C (1991) The control of the production process of phytoplankton by the physical structure of the aquatic environment with special reference to its optical properties. Aquat Sci 53:136–186

    Article  Google Scholar 

  • Raven JA, Geider RJ (2003) Adaptation, acclimation and regulation in algal phtosynthesis. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer Academic Publishers, Dordrecht, pp 385–412

    Chapter  Google Scholar 

  • Rivkin RB (1990) Photoadaptation in marine phytoplankton: variations in ribulose 1, 5-bisphosphate activity. Mar Ecol Prog Ser 62:61–72

    Article  CAS  Google Scholar 

  • Rodriguez F, Chauton M, Johnsen G, Andresen K, Olsen LM, Zapata M (2006) Photoacclimation in phytoplankton: implications for biomass estimates, pigment functionality and chemotaxonomy. Mar Biol 148:963–971

    Article  Google Scholar 

  • Röttgers R, Gehnke S (2012) Measurement of light absorption by aquatic particles: improvement of the quantitative filter technique by use of an integrating sphere approach. Appl Opt 51:1336–1351

    Article  PubMed  Google Scholar 

  • Ruban A, Lavaud J, Rousseau B, Guglielmi G, Horton P, Etienne AL (2004) The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynth Res 82:165–175

    Article  CAS  PubMed  Google Scholar 

  • Sakshaug E, Demers S, Yentsch CM (1987) Thalassiosira oceanica and T. Pseudonana: two different photoadaptational responses. Mar Ecol Prog Ser 41:275–282

    Article  Google Scholar 

  • Sakshaug E, Andresen K, Kiefer DA (1989) A steady state description of growth and light absorption in the marine planktonic diatom Skeletonema costatum. Limnol Oceanogr 34:198–205

    Article  Google Scholar 

  • Six C, Finkel ZV, Rodriguez F, Marie D, Partensky F, Campbell DA (2008) Contrasting photoacclimation costs in ecotypes of the marine eukaryotic picoplankter ostreococcus. Limnol Oceanogr 53:255

    Article  CAS  Google Scholar 

  • Stomp M, Huisman J, Stal LJ, Matthijs HC (2007) Colorful niches of phototrophic microorganisms shaped by vibrations of the water molecule. ISME J 1:271–282

    CAS  PubMed  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, Le Floch E, Harris GN, Leonardos N, Geider RJ (2007) Different strategies of photoacclimation by two strains of Emiliania huxleyi (haptophyta). J Phycol 43:1209–1222

    Article  CAS  Google Scholar 

  • Sukenik A, Bennett J, Falkowski P (1987) Light-saturated photosynthesis limitation by electron transport or carbon fixation? Biochimica et Biophysica Acta (BBA)-Bioenerg 891:205–215

  • Van Heukelem L, Thomas CS (2001) Computer-assisted high-performance liquid chromatography method development with applications to the isolation and analysis of phytoplankton pigments. J Chromatogr A 910:31–49

    Article  PubMed  Google Scholar 

  • Vass I, Styring S (1991) PH-dependent charge equilibria between tyrosine-d and the S states in photosystem II. Estimation of relative midpoint redox potentials. Biochemistry 30:830–839

    Article  CAS  PubMed  Google Scholar 

  • Vass I, Styring S, Hundal T, Koivuniemi A, Aro E, Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci 89:1408–1412

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992

    Article  CAS  Google Scholar 

  • West NJ, Scanlan DJ (1999) Niche-partitioning of prochlorococcus populations in a stratified water column in the eastern north atlantic ocean. Appl Environ Microbiol 65:2585–2591

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wright SW, Jeffrey SW, Mantoura RFC (1997) Phytoplankton pigments in oceanography: guidelines to modern methods. UNESCO Publishing, Paris

    Google Scholar 

  • Wu H, Cockshutt AM, McCarthy A, Campbell DA (2011) Distinctive photosystem II photoinactivation and protein dynamics in marine diatoms. Plant Physiol 156:2184–2195

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu H, Roy S, Alami M, Green BR, Campbell DA (2012) Photosystem II photoinactivation, repair, and protection in marine centric diatoms. Plant Physiol 160:464–476

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu Y, Jeans J, Suggett D, Finkel Z, Campbell DA (2014) Large centric diatoms allocate more cellular nitrogen to photosynthesis to counter slower RUBISCO turnover rates. Front Mar Sci. doi:10.3389/fmars.2014.00068

    Google Scholar 

  • Young JN, Goldman JAL, Kranz SA, Tortell PD, Morel FMM (2015) Slow carboxylation of Rubisco constrains the maximum rate of carbon fixation during Antarctic phytoplankton blooms. New Phytol 205:172–181

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are indebted to Carina Poulin, Mariette Lambert, Rosalie Parent and Patrick Cliche for their valuable support during experiments, and Audrey Barnett for processing the fluorescence induction data. We also want to thank the two anonymous reviewers for their suggestions to improve this manuscript.

Author information

Authors and Affiliations

  1. Canada Research Chair in Earth Observation and Phytoplankton Ecophysiology, Université de Sherbrooke, Sherbrooke, QC, J1K 2R1, Canada

    Jennifer Marie-Rose Vandenhecke & Yannick Huot

  2. Department of Chemistry & Biochemistry, Mount Allison University, Sackville, NB, E4L 1G7, Canada

    Jake Bastedo, Amanda M. Cockshutt & Douglas A. Campbell

Authors
  1. Jennifer Marie-Rose Vandenhecke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jake Bastedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amanda M. Cockshutt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Douglas A. Campbell
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yannick Huot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer Marie-Rose Vandenhecke.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Marie-Rose Vandenhecke, J., Bastedo, J., Cockshutt, A.M. et al. Changes in the Rubisco to photosystem ratio dominates photoacclimation across phytoplankton taxa. Photosynth Res 124, 275–291 (2015). https://doi.org/10.1007/s11120-015-0137-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-015-0137-6

Keywords

Search

Navigation