Increased CO2 and iron availability effects on carbon assimilation and calcification on the formation of Emiliania huxleyi blooms in a coastal phytoplankton community

Environmental and Experimental Botany - Tập 148 - Trang 47-58 - 2018
M. Rosario Lorenzo1, Concepción Iñiguez1, Jorun K. Egge2, Aud Larsen2,3, Stella A. Berger4, Candela García-Gómez1, María Segovia1
1Department of Ecology, Faculty of Sciences, University of Málaga, Bulevar Louis Pasteur s/n, Málaga, 29071, Spain
2Department of Biology, Thormøhlensgt. 53A/B, University of Bergen, 5020, Bergen, Norway
3Uni Research Environment, Nygårdsgaten 112, 5008, Bergen, Norway
4Department of Experimental Limnology, Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Alte Fischerhütte2, 16775, Stechlin, Germany

Tài liệu tham khảo

Bach, 2013, Dissecting the impact of CO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyi, New Phytol., 199, 121, 10.1111/nph.12225 Beardall, 2002, Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation, Funct. Plant Biol., 29, 335, 10.1071/PP01195 Beardall, 2004, The potential effects of global climate change on microalgae photosynthesis, growth and ecology, Phycologia, 43, 26, 10.2216/i0031-8884-43-1-26.1 Beaufort, 2011, Sensitivity of coccolithophores to carbonate chemistry and ocean acidification, Nature, 476, 80, 10.1038/nature10295 Behrenfeld, 2013, Photophysiological expressions of iron stress in phytoplankton, Ann. Rev. Mar. Sci., 5, 217, 10.1146/annurev-marine-121211-172356 Bellerby, 2008, Marine ecosystem community carbon and nutrient uptake stoichiometry under varying ocean acidification during the PeECE III experiment, Biogeosciences, 5, 1517, 10.5194/bg-5-1517-2008 Boudreau, 1997 Boyd, 2012, Understanding the responses of ocean biota to a complex matrix of cumulative anthropogenic change, Mar. Ecol. Prog. Ser., 470, 125, 10.3354/meps10121 Boyd, 2016, Physiological responses of a Southern Ocean diatom to complex future ocean conditions, Nat. Clim. Chang., 6, 207, 10.1038/nclimate2811 Cassar, 2004, Bicarbonate uptake by southern ocean phytoplankton, Global Biogeochem. Cycles, 18, 1, 10.1029/2003GB002116 Colman, 2002, The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae, Funct. Plant Biol., 29, 261, 10.1071/PP01184 Czerny, 2013, Implications of elevated CO2 on pelagic carbon fluxes in an arctic mesocosm study-an elemental mass balance approach, Biogeosciences, 10, 3109, 10.5194/bg-10-3109-2013 De Bodt, 2010, Individual and interacting effects of pCO2 and temperature on Emiliania huxleyi calcification: study of the calcite production, the coccolith morphology and the coccosphere size, Biogeosciences, 7, 1401, 10.5194/bg-7-1401-2010 Delille, 2005, Response of primary production and calcification to changes of pCO2 during experimental blooms of the coccolithophorid Emiliania huxleyi, Global Biogeochem. Cycles, 19, 1, 10.1029/2004GB002318 Doney, 2009, Ocean Acidification: a critical emerging problem for the ocean sciences, Oceanography, 22, 16, 10.5670/oceanog.2009.93 Egge, 1994, Blooms of phytoplankton including Emiliania huxleyi (Haptophyta): Effect of nutrient supply in different N:P ratios, Sarsia, 79, 333, 10.1080/00364827.1994.10413565 Egge, 2009, Primary production during nutrient-induced blooms at elevated CO2 concentrations, Biogeosciences, 6, 877, 10.5194/bg-6-877-2009 Egleston, 2010, Revelle revisited: buffer factors that quantify the response of ocean chemistry to changes in DIC and alkalinity, Global Biogeochem. Cycles, 24, GB1002, 10.1029/2008GB003407 Elzenga, 2000, The role of extracellular carbonic anhydrase activity in inorganic carbon utilization of Phaeocystis globosa (Prymnesiophyceae): A comparison with other marine algae using the isotopic disequilibrium technique, Limnol. Oceanogr., 45, 372, 10.4319/lo.2000.45.2.0372 Engel, 2005, Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments, Limnol. Oceanogr., 50, 493, 10.4319/lo.2005.50.2.0493 Engel, 2008, Effects of CO2 on particle size distribution and phytoplankton abundance during a mesocosm bloom experiment (PeECE II), Biogeosciences, 5, 509, 10.5194/bg-5-509-2008 Engel, 2013, CO2 increases 14C primary production in an Arctic plankton community, Biogeosciences, 10, 1291, 10.5194/bg-10-1291-2013 Espie, 1986, Inorganic carbon uptake during photosynthesis, Plant Physiol., 3, 863, 10.1104/pp.80.4.863 Feng, 2010, Interactive effects of iron, irradiance and CO2 on Ross Sea phytoplankton, Deep. Res. Part I Oceanogr. Res. Pap., 57, 368, 10.1016/j.dsr.2009.10.013 Field, 2011 Field, 1998, Primary production of the biosphere: integrating terrestrial and oceanic components, Science, 281, 237, 10.1126/science.281.5374.237 Findlay, 2011, Determinants of the PIC:POC response in the coccolithophore Emiliania huxleyi under future ocean acidification scenarios, Limnol. Oceanogr., 56, 1168, 10.4319/lo.2011.56.3.1168 Flynn, 2012, Changes in pH at the exterior surface of plankton with ocean acidification, Nat. Clim. Chang., 2, 510, 10.1038/nclimate1489 Giordano, 2005, CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution, Annu. Rev. Plant Biol., 56, 99, 10.1146/annurev.arplant.56.032604.144052 Herfort, 2003, Acquisition and use of bicarbonate by Emiliania huxleyi, New Phytol., 156, 427, 10.1046/j.1469-8137.2002.00523.x Holtz, 2015, Numerical cell model investigating cellular carbon fluxes in Emiliania huxleyi, J. Theor. Biol., 364, 305, 10.1016/j.jtbi.2014.08.040 Hoppe, 2013, Iron limitation modulates ocean acidification effects on Southern Ocean phytoplankton communities, PLoS One, 8, 10.1371/annotation/c3c66438-6fc0-4b1a-ba1e-9ea637695e8b Hutchins, 2009, Nutrient cycles and marine microbes in a CO2-enriched ocean, Oceanography, 22, 128, 10.5670/oceanog.2009.103 IPCC, 2013 Johnson, 1982, Carbon dioxide hydration and dehydrationkinetics in seawater, Limnol. Oceanogr., 27, 849, 10.4319/lo.1982.27.5.0849 Kim, 2006, The effect of seawater CO2 concentration on growth of a natural phytoplankton assemblage in a controlled mesocosm experiment, Limnol. Oceanogr., 51, 1629, 10.4319/lo.2006.51.4.1629 Kranz, 2015, Low temperature reduces the energetic requirement for the CO2 concentrating mechanism in diatoms, New Phytol., 205, 192, 10.1111/nph.12976 Langer, 2009, Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry, Biogeosci. Discuss., 6, 4361, 10.5194/bgd-6-4361-2009 Loebl, 2010, Physiological basis for high resistance to photoinhibition under nitrogen depletion in Emiliania huxleyi, Limnol. Oceanogr., 55, 2150, 10.4319/lo.2010.55.5.2150 Mackey, 2015, Response of photosynthesis to ocean acidification, Oceanography, 28, 74, 10.5670/oceanog.2015.33 Martin, 2006, Bicarbonate transport and extracellular carbonic anhydrase activity in Bering Sea phytoplankton assemblages: results from isotope disequilibrium experiments, Limnol. Oceanogr., 51, 2111, 10.4319/lo.2006.51.5.2111 Meyer, 2015, Reviews and Syntheses: responses of coccolithophores to ocean acidification: a meta-analysis, Biogeosciences, 12, 1671, 10.5194/bg-12-1671-2015 Millero, 2009, Effect of ocean acidification on the speciation of metals in seawater, Oceanography, 22, 72, 10.5670/oceanog.2009.98 Muller, 2014, Dynamic energy budget modeling reveals the potential of future growth and calcification for the coccolithophore Emiliania huxleyi in an acidified ocean, Glob. Chang. Biol., 20, 2031, 10.1111/gcb.12547 Nimer, 1992, Utilization of inorganic carbon by the coccolithophorid Emiliania huxleyi (Lohmann) Kamptner, New Phytol., 120, 153, 10.1111/j.1469-8137.1992.tb01068.x Nimer, 1994, Extra- and intra-cellular carbonic anhydrase in relation to culture age in a high-calcifying strain of Emiliania huxleyi Lohmann, New Phytol., 126, 601, 10.1111/j.1469-8137.1994.tb02954.x Paasche, 2002, A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae) with particular reference to growth, coccolith formation, and calcification- photosynthesis interacions, Phycol. Rev., 40, 503, 10.2216/i0031-8884-40-6-503.1 Paulino, 2013, Elemental stoichiometry of marine particulate matter measured by wavelength dispersive X-ray fluorescence (WDXRF) spectroscopy, J. Mar. Biol. Assoc. United Kingdom, 93, 2003, 10.1017/S0025315413000635 Read, 2013, Pan genome of the phytoplankton Emiliania underpins its global distribution, Nature, 499, 209, 10.1038/nature12221 Richier, 2014, Phytoplankton responses and associated carbon cycling during shipboard carbonate chemistry manipulation experiments conducted around Northwest European shelf seas, Biogeosciences, 11, 4733, 10.5194/bg-11-4733-2014 Riebesell, 2011, Effects of ocean acidification on pelagic organisms and ecosystems, 99 Riebesell, 2000, Reduced calcification of marine plankton in response to increased atmospheric CO2, Nature, 10.1038/35030078 Riebesell, 2007, Enhanced biological carbon consumption in a high CO2 ocean, Nature, 450, 545, 10.1038/nature06267 Riebesell, 2008, Comment on Phytoplankton calcification in a high-CO2 world, Science, 322 Robbins, 2010, CO2calc- A user friendly seawater carbon calculator for Windows, Mac OSX and iOS (iPhone), 1280, 10.3133/ofr20101280 Rokitta, 2012, Effects of CO2 and their modulation by light in the life-cycle stages of the coccolithophore Emiliania huxleyi, Limnol. Oceanogr., 57, 607, 10.4319/lo.2012.57.2.0607 Rokitta, 2012, Ocean acidification affects redox-balance and ion-homeostasis in the life-cycle stages of Emiliania huxleyi, PLoS One, 7, e52212, 10.1371/journal.pone.0052212 Rost, 2003, Carbon acquisition of bloom-forming marine phytoplankton, Limnol. Oceanogr., 48, 55, 10.4319/lo.2003.48.1.0055 Rost, 2006, Carbon acquisition of marine phytoplankton: effect of photoperiod length, Limnol. Oceanogr., 51, 12, 10.4319/lo.2006.51.1.0012 Rost, 2007, Isotope disequilibrium and mass spectrometric studies of inorganic carbon acquisition by phytoplankton, Limnol. Oceanogr. Methods, 5, 328, 10.4319/lom.2007.5.328 Saito, 2008, Some thoughts on the concept of colimitation: three definitions and the importance of bioavailability, Limnol. Oceanogr., 53, 276, 10.4319/lo.2008.53.1.0276 Schartau, 2007, Modelling carbon overconsumption and the formation of extracellular particulate organic carbon, Biogeosciences, 4, 433, 10.5194/bg-4-433-2007 Schulz, 2004, Effect of trace metal availability on coccolithophorid calcification, Nature, 430, 673, 10.1038/nature02631 Schulz, 2009, CO2 perturbation esperiments: similarities and differences between dissolved inorganic carbon and total alkalinity manipulations, Biogeosciences, 6, 2145, 10.5194/bg-6-2145-2009 Segovia, 2017, Iron availability modulates the effects of future CO2 levels within the marine planktonic food web, Mar. Ecol. Prog. Ser., 565, 17, 10.3354/meps12025 Segovia, 2018, Physiological stress response associated with elevated CO2 and dissolved iron in a phytoplankton community dominated by the coccolithophore Emiliania huxleyi, Mar. Ecol. Prog. Ser., 586, 73, 10.3354/meps12389 Shaked, 2012, Disassembling iron availability to phytoplankton, Front. Microbiol., 3, 123, 10.3389/fmicb.2012.00123 Shi, 2010, Effect of ocean acidification on iron availability to marine phytoplankton, Science, 327, 676, 10.1126/science.1183517 Steemann Nielsen, 1952, The use of radioactive (14C) for measuring organic production in the sea, J. du Cons./Cons. Perm. Int. pour l’Exploration la Mer, 18, 117, 10.1093/icesjms/18.2.117 Stojkovic, 2013, CO2-concentrating mechanisms in three southern hemisphere strains of Emiliania huxleyi, J. Phycol., 49, 670, 10.1111/jpy.12074 Suffrian, 2011, Cellular pH measurements in Emiliania huxleyi reveal pronounced membrane proton permeability, New Phytol., 190, 595, 10.1111/j.1469-8137.2010.03633.x Sugie, 2013, Synergistic effects of pCO2 and iron availability on nutrient consumption ratio of the Bering Sea phytoplankton community, Biogeosci. Discuss., 10.5194/bg-10-6309-2013 Sunda, 2010, Oceans. Iron and the carbon pump, Science, 327, 654, 10.1126/science.1186151 Taylor, 2012, Proton channels in algae: reasons to be excited, Trends Plant Sci., 17, 675, 10.1016/j.tplants.2012.06.009 Tortell, 2002, Sources of inorganic carbon for phytoplankton in the eastern Subtropical and Equatorial Pacific Ocean, Limnol. Oceanogr., 47, 1012, 10.4319/lo.2002.47.4.1012 Tortell, 2008, CO2 sensitivity of southern ocean phytoplankton, Geophys. Res. Lett., 35, L04605, 10.1029/2007GL032583 Tortell, 2010, Inorganic carbon ttilization by ross Sea phytoplankton across natural and experimental CO2 gradients, J. Phycol., 46, 433, 10.1111/j.1529-8817.2010.00839.x Tortell, 2013, Inorganic C utilization and C isotope fractionation by pelagic and sea ice algal assemblages along the antarctic continental shelf, Mar. Ecol. Prog. Ser., 483, 47, 10.3354/meps10279 Yang, 2012, Physiological responses of the marine diatom Thalassiosira pseudonana to increased pCO2 and seawater acidity, Mar. Environ. Res., 79, 142, 10.1016/j.marenvres.2012.06.002 Yoshimura, 2013, Impacts of elevated CO2 on particulate and dissolved organic matter production: microcosm experiments using iron-deficient plankton communities in open subarctic waters, J. Oceanogr., 69, 601, 10.1007/s10872-013-0196-2 Yoshimura, 2014, Organic matter production response to CO2 increase in open subarctic plankton communities: comparison of six microcosm experiments under iron-limited and −enriched bloom conditions, Deep. Res. Part I Oceanogr. Res. Pap., 94, 1, 10.1016/j.dsr.2014.08.004 Zondervan, 2001, Decreasing marine biogenic calcification: a negative feedback on rising atmospheric pCO2, Global Biogeochem. Cycles, 15, 507, 10.1029/2000GB001321 Zondervan, 2002, Effect of CO2 concentration on the PIC/POC ratio in the coccolithophore Emiliania huxleyi grown under light-limiting conditions and different daylengths, J. Exp. Mar. Biol. Ecol., 272, 55, 10.1016/S0022-0981(02)00037-0