Differential responses of growth and photosynthesis in the marine diatom Chaetoceros muelleri to CO₂ and light availability

REFERENCES

• Amoroso G., Weber C., Sultemeyer D. & Fock H. 1996. Intracellular carbonic anhydrase activities in Dunaliella tertiolecta (Butcher) and Chlamydomonas reinhardtii (Dangeard) in relation to inorganic carbon concentration during growth: Further evidence for the existence of two distinct carbonic anhydrases associated with the chloroplasts. Planta 199: 177–184.
   Web of Science ®Google Scholar
• Andria J.R., Perez-Lloren J.L. & Vergara J.J. 1999. Mechanisms of inorganic carbon acquisition in Gracilaria gaditana nom. prov. (Rhodophyta). Planta 208: 564–573.
   Web of Science ®Google Scholar
• Axelsson L. 1988. Changes in pH as a measure of photosynthesis by marine macroalgae. Marine Biology 97: 278–294.
   Web of Science ®Google Scholar
• Axelsson L. & Uusitalo J. 1988. Carbon acquisition strategies for marine macroalgae. Marine Biology 97: 295–300.
   Web of Science ®Google Scholar
• Badger M.R. & Schreiber U. 1993. Effects of inorganic carbon accumulation on photosynthetic oxygen reduction and cyclic electron flow in the Cyanobacterium Synechococcus Pcc7942. Photosynthesis Research 37(3): 177–191.
   Web of Science ®Google Scholar
• Baker N.R. 2008. Chlorophyll fluorescence: a probe of photosynthesis. In Vivo Annual Review of Plant Biology 59: 89–111.
   PubMed Web of Science ®Google Scholar
• Beardall J. 1991. Effects of photon flux-density on the CO2-concentrating mechanism of the Cyanobacterium Anabaena variabilis. Journal of Plankton Research 13: 133–141.
   Web of Science ®Google Scholar
• Beardall J. & Giordano M. 2002. Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation. Functional Plant Biology 29: 335–347.
   PubMed Web of Science ®Google Scholar
• Beardall J. & Raven J.A. 2004. The potential effects of global climate change on microalgal photosynthesis, growth and ecology. Phycologia 43: 26–40.
   Web of Science ®Google Scholar
• Beardall J., Mukerji D., Glover H.E. & Morris I. 1976. Path of carbon in photosynthesis by marine phytoplankton. Journal of Phycology 12: 409–417.
   Web of Science ®Google Scholar
• Beardall J., Beer S. & Raven J.A. 1998. Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance. Botanica Marina 41: 113–123.
   Web of Science ®Google Scholar
• Beardall J., Johnston A. & Raven J. 1998b. Environmental regulation of CO2-concentrating mechanisms in microalgae. Canadian Journal of Botany 76: 1010–1017.
   Google Scholar
• Bown A.W. 1985. CO2 and intracellular pH. Plant, Cell & Environment 459–465.
   Google Scholar
• Burns N.R., Mackenzie T.D.B. & Campbell D.A. 2006. Inorganic carbon repletion constrains steady-state light acclimation in the cyanobacterium Synechococcus elongatus. Journal of Phycology 42: 610–621.
   Web of Science ®Google Scholar
• Cabantchik Z. & Greger R. 1992. Chemical probes for anion transporters of mammalian cell membranes. American Journal of Physiology Cell Physiology 262: C803–C827.
   Google Scholar
• Chen C.Y. & Durbin E.G. 1994. Effects of pH on the growth and carbon uptake of marine phytoplankton. Marine Ecology Progress Series 109: 83–94.
   Web of Science ®Google Scholar
• Choo K.S., Snoeijs P. & Pedersen M. 2002. Uptake of inorganic carbon by Cladophora glomerata (Chlorophyta) from the Baltic Sea. Journal of Phycology 38: 493–502.
   Web of Science ®Google Scholar
• Coleman J.R. & Colman B. 1981. Inorganic carbon accumulation and photosynthesis in a blue-green alga as a function of external pH. Plant Physiology 67: 917–921.
   PubMed Web of Science ®Google Scholar
• Dixon G.K., Brownlee C. & Merrett M.J. 1989. Measurement of internal pH in the coccolithophore Emiliania huxleyii using 2,7-bis-(2-fluorescein) acetoxymethyl ester and digital imaging microscopy. Planta 178: 443–449.
   PubMed Web of Science ®Google Scholar
• Drechsler Z. & Beer S. 1991. Utilization of inorganic carbon by Ulva lactuca. Plant Physiology 97: 1439–1444.
   PubMed Web of Science ®Google Scholar
• Eilers P.H.C. & Peeters J.C.H. 1988. A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecological Modelling 42(3–4): 199–215.
   Web of Science ®Google Scholar
• Engel A., Zondervan I., Aerts K., Beaufort L., Benthien A., Chou L., Delille B., Gattuso J., Harlay J. & Heemann C. 2005. Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments. Limnology and Oceanography 50: 493–507.
   Web of Science ®Google Scholar
• Falk S. & Palmqvist K. 1992. Photosynthetic light utilization efficiency, photosystem-II heterogeneity, and fluorescence quenching in Chlamydomonas reinhardtii during the induction of the CO2-concentrating mechanism. Plant Physiology 100: 685–691.
   Web of Science ®Google Scholar
• Falkowski P.G., Owens T.G., Ley A.C. & Mauzerall D. 1981. Effects of growth irradiance levels on the ratio of reaction centers in 2 species of marine phytoplankton. Plant Physiology 68: 969–973.
   PubMed Web of Science ®Google Scholar
• Fujiki T., Suzue T. & Kimoto H. 2007. Photosynthetic electron transport in Dunaliella tertiolecta (Chlorophyceae) measured by fast repetition rate fluorometry: relation to carbon assimilation. Journal of Plankton Research 29: 199–208.
   Web of Science ®Google Scholar
• Gattuso J. & Lavigne H. 2009. Technical note: approaches and software tools to investigate the impact of ocean acidification. Biogeosciences 6: 2121–2133.
   Web of Science ®Google Scholar
• Geel C., Versluis W. & Snel J. 1997. Estimation of oxygen evolution by marine phytoplankton from measurement of the efficiency of photosystem II electron flow. Photosynthesis Research 51: 61–70.
   Web of Science ®Google Scholar
• Gilmour D.J., Hipkins M.F., Webber A.N., Baker N.R. & Al E. 1985. The effect of ionic stress on photosynthesis in Dunaliella tertiolecta. Planta 163: 250–256.
   Web of Science ®Google Scholar
• Giordano M., Beardall J. & Raven J.A. 2005. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annual Review of Plant Physiology 56: 99–131.
   Google Scholar
• Gordillo F., Jimenez C., Chavarria J. & Niell X. 2001. Photosynthetic acclimation to photon irradiance and its relation to chlorophyll fluorescence and carbon assimilation in the halotolerant green alga Dunaliella viridis. Photosynthesis Research 68: 225–235.
   Web of Science ®Google Scholar
• Granum E., Raven J.A. & Leegood R.C. 2005. How do marine diatoms fix 10 billion tonnes of inorganic carbon per year? Canadian Journal of Botany 83: 898–908.
   Google Scholar
• Heber U. 2002. Irrungen, Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynthesis Research 73: 223–231.
   PubMed Web of Science ®Google Scholar
• Jassby A. & Platt T. 1976. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnology and Oceanography 21: 540–547.
   Web of Science ®Google Scholar
• Johnston A.M., Raven J.A., Beardall J. & Leegood R.C. 2001. Carbon fixation — photosynthesis in a marine diatom. Nature 412: 40–41.
   PubMed Web of Science ®Google Scholar
• Kallas T. & Castenholz R.W. 1982. Rapid transient growth at low pH in the Cyanobacterium Synechococcus sp. Journal of Bacteriology 149: 237–246.
   Web of Science ®Google Scholar
• Katzman G.L., Katzman G.L., Carlson S., Marcus Y., Moroney J. & Togasaki R. 1994. Carbonic anhydrase activity in isolated chloroplasts of wild-type and high CO2-dependent mutants of Chlamydomonas reinhardtii is studied by a new assay. Plant Physiology 105: 1197–1202.
   PubMed Web of Science ®Google Scholar
• Krause G. & Weis E. 1991. Chlorophyll fluorescence and photosynthesis — the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42: 313–349.
   Web of Science ®Google Scholar
• Kubler J.E. & Raven J.A. 1995. The interaction between inorganic carbon acquisition and light supply in Palmaria palmata (Rhodophyta). Journal of Phycology 31: 369–375.
   Web of Science ®Google Scholar
• Lavaud J. 2007. Fast regulation of photosynthesis in diatoms: mechanisms, evolution and ecophysiology. Global Science Books — Functional Plant Science and Biotechnology 1: 267–287.
   Google Scholar
• Lavigne H., Proye A. & Gattuso J.P. 2008. Seacarb 2.0, an R-package to calculated parameters of the seawater carbonate system. Online available at: http://cran.r-projects.org/web/packages/seacarb/index.html.
   Google Scholar
• Leonardos N. & Geider R. 2004. Effects of nitrate: phosphate supply ratio and irradiance on the C:N:P stoichiometry of Chaetoceros muelleri. European Journal of Phycology 39: 173–180.
   Web of Science ®Google Scholar
• Leonardos N. & Geider R. 2005. Elemental and biochemical composition of Rhinomonas reticulata (Cryptophyta) in relation to light and nitrate-to-phosphate supply ratios. Journal of Phycology 41: 567–576.
   Web of Science ®Google Scholar
• Lundholm N., Hansen P.J. & Kotaki Y. 2004. Effect of pH on growth and domoic acid production by potentially toxic diatoms of the genera Pseudo-nitzschia and Nitzschia. Marine Ecology Progress Series 273: 1–15.
   Web of Science ®Google Scholar
• Maberly S. 1990. Exogenous sources of inorganic carbon for photosynthesis in marine macroalgae. Journal of Phycology 26: 439–449.
   Web of Science ®Google Scholar
• Merrett M.J., Nimer N.A. & Dong L.F. 1996. The utilization of bicarbonate ions by the marine microalga Nannochloropsis oculata (Droop) Hibberd. Plant, Cell & Environment 19: 478–484.
   Web of Science ®Google Scholar
• Michelet B. & Boutry M. 1995. The plasma membrane H+-ATPase — a highly regulated enzyme with multiple physiological. Plant Physiology 108: 1–6.
   PubMed Web of Science ®Google Scholar
• Middelboe A. & Hansen P. 2007. Direct effects of pH and inorganic carbon on macroalgal photosynthesis and growth. Marine Biology Research 3: 134–144.
   Web of Science ®Google Scholar
• Miyake C. & Yokota A. 2001. Cyclic flow of electrons within PSII in thylakoid membranes. Plant Cell Physiology 42: 508–515.
   PubMed Web of Science ®Google Scholar
• Moroney J., Husic H. & Tolbert N. 1985. Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiology 79: 177–183.
   PubMed Web of Science ®Google Scholar
• Moroney J., Tolbert N.E. & Sears B. 1986. Complementation of the inorganic carbon concentrating mechanism of Chlamydomonas reinhardtii. Molecular and General Genetics 204: 199–203.
   Google Scholar
• Nielsen L., Lundholm N. & Hansen P. 2007. Does irradiance influence the tolerance of marine phytoplankton to high pH? Marine Biology Research 3: 446–453.
   Web of Science ®Google Scholar
• Nimer N.A., Brownlee C. & Merrett M.J.R. 1994. Carbon dioxide availability, intracellular pH and growth rate of the coccolithophore Emiliania huxleyi. Marine Ecology Progress Series 109: 257–262.
   Web of Science ®Google Scholar
• Nimer N., Igesias-Rodriguez M. & Merrett M. 1997. Bicarbonate utilization by marine phytoplankton species. Journal of Phycology 33: 625–631.
   Web of Science ®Google Scholar
• Niyogi K. 2000. Safety valves for photosynthesis. Current Opinions in Plant Biology 3: 455–460.
   PubMed Web of Science ®Google Scholar
• Palmqvist K., Sundblad L.G., Wingsle G. & Samuelsson G. 1990. Acclimation of photosynthetic light reactions during induction of inorganic carbon accumulation in the green alga Chlamydomonas reinhardtii. Plant Physiology 94: 357–366.
   PubMed Web of Science ®Google Scholar
• Price G. & Badger M. 1989. Ethoxyzolamide inhibition of CO2 uptake in the cyanobacterium Synechococcus Pcc7942 without apparent inhibition of internal carbonic-anhydrase activity. Plant Physiology 89: 37–43.
   Web of Science ®Google Scholar
• Quigg A. & Beardall J. 2003. Protein turnover in relation to maintenance metabolism at low photon flux in two marine microalgae. Plant, Cell & Environment 26: 693–703.
   Web of Science ®Google Scholar
• Quigg A., Kevekorder K., Raven J.A. & Beardall J. 2006. Limitations on microalgal growth at very low photon fluence rates: the role of energy slippage. Photosynthesis Research 88: 299–310.
   PubMed Web of Science ®Google Scholar
• Ramus J., Beale S.I., Mauzerall D. & Howard K. 1976. Changes in photosynthetic pigment concentration in seaweeds as a function of water depth. Marine Biology 37: 223–229.
   Web of Science ®Google Scholar
• Raven J.A. 1991. Implications of inorganic carbon utilization — ecology, evolution, and geochemistry. Canadian Journal of Botany 69: 908–924.
   Google Scholar
• Raven J.A. 2003. Inorganic carbon concentrating mechanisms in relation to the biology of algae. Photosynthesis Research 77: 155–171.
   Web of Science ®Google Scholar
• Raven J.A. & Newman J.R. 1994. Requirement for carbonic-anhydrase activity in processes other than photosynthetic inorganic carbon assimilation. Plant, Cell & Environment 17: 123–130.
   Web of Science ®Google Scholar
• Raven J.A., Beardall J., Johnston A.M. & Kubler J.E. 1995. Inorganic carbon acquisition by Hormosira banksii (Phaeophyta: Fucales) and its epiphyte Notheiaanomala (Phaeophyta: Fucales). Phycologia 34: 267–277.
   Web of Science ®Google Scholar
• Raven J.A., Kubler J.E. & Beardall J. 2000. Put out the light, and then put out the light. Journal of the Marine Biological Association of the United Kingdom 80: 1–25.
   Web of Science ®Google Scholar
• Raven J.A., Giordano M. & Beardall J. 2007. Insights into the evolution of CCM from comparisons with other resource acquisition and assimilation processes. Physiologia Plantarum 133: 4–14.
   Web of Science ®Google Scholar
• Reinfelder J.R., Kraepiel A.M.L. & Morel F.M.M. 2000. Unicellular C4 photosynthesis in a marine diatom. Nature 407: 996–999.
   PubMed Web of Science ®Google Scholar
• Reinfelder J.R., Milligan A.J. & Morel F.M.M. 2004. The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiology 135: 1–6.
   Web of Science ®Google Scholar
• Riebesell U. 2000. Photosynthesis — carbon fix for a diatom. Nature 407: 959–960.
   PubMed Web of Science ®Google Scholar
• Riebesell U. 2004. Effects of CO2 enrichment on marine phytoplankton. Journal of Oceanography 60: 719–729.
   Web of Science ®Google Scholar
• Rost B., Zondervan I. & Wolf-Gladrow D. 2008. Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions. Marine Ecology Progress Series 373: 227–237.
   Web of Science ®Google Scholar
• Schulz K., Barcelos e Ramos J., Zeebe J. & Riebesell U. 2009. CO2 perturbation experiments: similarities and differences between dissolved inorganic carbon and total alkalinity manipulations. Biogeosciences 6: 2145–2153.
   Web of Science ®Google Scholar
• Shi D., Xu Y. & Morel F. 2009. Effects of the pH/pCO2 control method on medium chemistry and phytoplankton growth. Biogeosciences 6: 1199–1207.
   Web of Science ®Google Scholar
• Smith F.A. & Raven J.A. 1979. Intracellular pH and its regulation. Annual Review of Plant Physiology 30: 289–311.
   Google Scholar
• Snoeijs P., Klenell M., Choo K.S., Comhaire I., Ray S. & Pedersen M. 2002. Strategies for carbon acquisition in the red marine macroalga Coccotylus truncatus from the Baltic Sea. Marine Biology 140: 435–444.
   Web of Science ®Google Scholar
• Spalding M.H., Spreitzer R.J. & Ogren W.L. 1983. Carbonic anhydrase deficient mutant of Chlamydomonas reinhardii requires elevated carbon-dioxide conentration for photoautotrophic growth. Plant Physiology 73: 268–272.
   Web of Science ®Google Scholar
• Spalding M.H., Critchley C. & Govindjee Orgren W.L. 1984. Influence of carbon-dioxide concentration during growth on fluorescence induction characteristics of the green alga Chlamydomonas reinhardii. Photosynthesis Research 5: 169–176.
   PubMed Web of Science ®Google Scholar
• Sukenik A., Bennett J. & Falkowski P.G. 1987. Light-saturated photosynthesis — limitation by electron-transport or carbon fixation. Biochimica et Biophysica Acta 891: 205–215.
   Web of Science ®Google Scholar
• Sukenik A., Tchernov D., Kaplan A., Huertas E., Lubian L.M. & Livne A. 1997. Uptake, efflux, and photosynthetic utilization of inorganic carbon by the marine eustigmatophyte Nannochloropsis sp. Journal of Phycology 33: 969–974.
   Web of Science ®Google Scholar
• Sultemeyer D., Amoroso G. & Fock H.P. 1995. Induction of intracellular carbonic-anhydrases during the adaptation to low inorganic carbon concentrations in wild-type and CA-1 mutant cells of Chlamydomonas reinhardtii. Planta 196: 217–224.
   Web of Science ®Google Scholar
• Ting C.S. & Owens T.G. 1993. Photochemical and nonphoto-chemical fluorescence quenching processes in the diatom Phaeodactylum tricornutum. Plant Physiology 101: 1323–1330.
   PubMed Web of Science ®Google Scholar
• Ting C.S. & Owens T.G. 1994. The effects of excess irradiance on photosynthesis in the marine diatom Phaeodactylum tricornutum. Plant Physiology 106: 763–770.
   PubMed Web of Science ®Google Scholar
• Tortell P.D., Reinfelder J.R. & Morel F.M.M. 1997. Active uptake of bicarbonate by diatoms. Nature 390: 243–244.
   PubMed Web of Science ®Google Scholar
• Tyrrell P.N., Kandasamy R.A., Crotty C.M. & Espie G.S. 1996. Ethoxyzolamide differentially inhibits CO2 uptake and Na+-independent and Na+-dependent HCO3- uptake in the cyanobacterium Synechococcus sp. UTEX 625. Plant Physiology 112: 79–88.
   Web of Science ®Google Scholar
• Wagner H., Jakob T. & Wilhelm C. 2006. Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytology 169: 95–108.
   PubMed Web of Science ®Google Scholar
• Xia J.R. & Gao K.S. 2003. Effects of doubled atmospheric CO2 concentration on the photosynthesis and growth of Chlorella pyrenoidosa cultured at varied levels of light. Fisheries Science 69: 767–771.
   Web of Science ®Google Scholar
• Young E., Beardall J. & Giordano M. 2001. Inorganic carbon acquisition by Dunaliella tertiolecta (Chlorophyta) involves external carbonic anhydrase and direct HCO3- utilization insensitive to the anion exchange inhibitor DIDS. European Journal of Phycology 36: 81–88.
   Web of Science ®Google Scholar
• Young E.B. & Beardall J. 2005. Modulation of photosynthesis and inorganic carbon acquisition in a marine microalga by nitrogen, iron, and light availability. Canadian Journal of Botany 83: 917–928.
   Google Scholar
• Zondervan I. 2007. The effects of light, macronutrients, trace metals and CO2 on the production of calcium carbonate and organic carbon in coccolithophores — a review. Deep Sea Research Part II 272: 521–537.
   Google Scholar
• Zou D.H., Gao K.S. & Xia J.R. 2003. Photosynthetic utilization of inorganic carbon in the economic brown alga, Hizikia fusiforme (Sargassaceae) from the South China Sea. Journal of Phycology 39: 1095–1100.
   Web of Science ®Google Scholar