Oceanography The Official Magazine of
The Oceanography Society
Volume 28 Issue 02

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Volume 28, No. 2
Pages 74 - 91

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Response of Photosynthesis to Ocean Acidification

By Katherine R.M. Mackey , J. Jeffrey Morris , François M.M. Morel , and Sven A. Kranz  
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Article Abstract

All phytoplankton and higher plants perform photosynthesis, where carbon dioxide is incorporated into biomass during cell growth. Ocean acidification (OA) has the potential to affect photosynthetic kinetics due to increasing seawater pCO2 levels and lower pH. The effects of increased CO2 are difficult to predict because some species utilize carbon concentrating mechanisms that buffer their sensitivity to ambient CO2 levels and require variable energy investments. Here, we discuss the current state of knowledge about the effects of increased CO2 on photosynthesis across marine photosynthetic taxa from cyanobacteria and single-celled eukaryotes to marine macrophytes. The analysis shows that photosynthetic responses to OA are relatively small for most investigated species and highly variable throughout taxa. This could suggest that the photosynthetic benefits of high CO2 are minor relative to the cell’s overall energy and material balances, or that the benefit to photosynthesis is counteracted by other negative effects, such as possible respiratory costs from low pH. We conclude with recommendations for future research directions, such as probing how other physiological processes respond to OA, the effects of multiple stressors, and the potential evolutionary outcomes of long-term growth under ocean acidification.

Citation

Mackey, K.R.M., J.J. Morris, F.M.M. Morel, and S.A. Kranz. 2015. Response of photosynthesis to ocean acidification. Oceanography 28(2):74–91, https://doi.org/10.5670/oceanog.2015.33.

Supplementary Materials

» Supplemental Table S1 (25 KB .csv file) A table of data used for Figure 2—data collected from studies that compared the indicated parameters at modern (~380 ppm) versus elevated (650–1,000 ppm) CO2.

» Data and Methods (http://www.bco-dmo.org/dataset/554221/data)
The raw data from the literature review, as well as methods used to compile and process those data, are archived at BCO-DMO.

References

Andersson, A.J., D.I. Kline, P.J. Edmunds, S.D. Archer, N. Bednaršek, R.C. Carpenter, M. Chadsey, P. Goldstein, A.G. Grottoli, T.P. Hurst, and others. 2015. Understanding ocean acidification impacts on organismal to ecological scales. Oceanography 28(2):16–27, https://doi.org/10.5670/oceanog.2015.27.

Anthony, K.R.N., D. Kline, G. Diaz-Pulido, S. Dove, and O. Hoegh-Guldberg. 2008. Ocean acidification causes bleaching and productivity loss in coral reef builders. Proceedings of the National Academy of Sciences of the United States of America 105:17,442–17,446, https://doi.org/10.1073/pnas.0804478105.

Bach, L.T., L.C.M. Mackinder, K.G. Schulz, G. Wheeler, D.C. Schroeder, C. Brownlee, and U. Riebesell. 2013. Dissecting the impact of CO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyi. New Phytologist 199:121–134, https://doi.org/10.1111/nph.12225.

Bach, L.T., U. Riebesell, and K.G. Schulz. 2011. Distinguishing between the effects of ocean acidification and ocean carbonation in the coccolithophore Emiliania huxleyi. Limnology and Oceanography 56:2,040–2,050, https://doi.org/10.4319/lo.2011.56.6.2040.

Badger, M.R., T.J. Andrews, S.M. Whitney, M. Ludwig, and D.C. Yellowlees. 1998. The diversity and co-evolution of Rubisco, plastids, pyrenoids and chloroplast-based CO2-concentrating mechanisms in the algae. Canadian Journal of Botany 76:1,052–1,071, https://doi.org/10.1139/b98-074.

Badger, M.R., and G.D. Price. 2003. CO2 concentrating mechanisms in cyanobacteria: Molecular components, their diversity and evolution. Journal of Experimental Botany 54:609–622, https://doi.org/10.1093/jxb/erg076.

Barcelos é Ramos, J., H. Biswas, K.G. Schulz, J. LaRoche, and U. Riebesell. 2007. Effect of rising atmospheric carbon dioxide on the marine nitrogen fixer Trichodesmium. Global Biogeochemical Cycles 21, GB2028, https://doi.org/10.1029/2006GB002898.

Beardall, J., and M. Giordano. 2002. Ecological implications of microalgal and cyanobacterial CCMs and their regulation. Functional Plant Biology 29:335–347, https://doi.org/10.1071/pp01195.

Beaufort, L., I. Probert, T. de Garidel-Thoron, E.M. Bendif, D. Ruiz-Pino, N. Metzl, C. Goyet, N. Buchet, P. Coupel, M. Grelaud, and others. 2011. Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476:80–83, https://doi.org/10.1038/nature10295.

Beer, S. 1994. Mechanisms of inorganic carbon acquisition in marine macroalgae (with special reference to the Chlorophyta). Progress in Phycological Research 10:179–207.

Berman-Frank, I., J. Erez, and A. Kaplan. 1998. Changes in inorganic carbon uptake during the progression of a dinoflagellate bloom in a lake ecosystem. Canadian Journal of Botany 76(6):1,043–1,051, https://doi.org/10.1139/b98-075.

Berman-Frank, I., P. Lundgren, Y.B. Chen, H. Küpper, Z. Kolber, B. Bergman, and P. Falkowski. 2001. Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294:1,534–1,537, https://doi.org/10.1126/science.1064082.

Böhme, H. 1998. Regulation of nitrogen fixation in heterocyst-forming cyanobacteria. Trends in Plant Science 3:346–351, https://doi.org/10.1016/S1360-1385(98)01290-4.

Brading, P., M.E. Warner, P. Davey, D. J. Smith, E.P. Achterberg, and D.J. Suggett. 2011. Differential effects of ocean acidification on growth and photosynthesis among phylotypes of Symbiodinium (Dinophyceae). Limnology and Oceanography 56(3): 927–938, https://doi.org/10.4319/lo.2011.56.3.0927.

Buitenhuis, E.T., H.J.W de Baar, and M.J.W. Veldhuis. 1999. Photosynthesis and calcification by Emiliania huxleyi (Prymnesiophyceae) as a function of inorganic carbon species. Journal of Phycology 35:949–959, https://doi.org/10.1046/j.1529-8817.1999.3550949.x.

Burkhardt, S., G. Amoroso, U. Riebesell, and D. Sultemeyer. 2001. CO2 and HCO3– uptake in marine diatoms acclimated to different CO2 concentrations. Limnology and Oceanography 46:1,378–1,391, https://doi.org/10.4319/lo.2001.46.6.1378.

Capone, D.G., J.A. Burns, J.P. Montoya, A. Subramaniam, C. Mahaffey, T. Gunderson, A.F. Michaels, and E.J. Carpenter. 2005. Nitrogen fixation by Trichodesmium spp.: An important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Global Biogeochemical Cycles 19, GB2024, https://doi.org/10.1029/2004GB002331.

Cassar, N., E.A. Laws, and B.N. Popp. 2006. Carbon isotopic fractionation by the marine diatom Phaeodactylum tricornutum under nutrient- and light-limited growth conditions. Geochimica et Cosmochimica Acta 70:5,323–5,335, https://doi.org/10.1016/j.gca.2006.08.024.

Chisholm, J.R.M. 2003. Primary productivity of reef-building crustose coralline algae. Limnology and Oceanography 48:1,376–1,387.

Collins, S., B. Rost, and T.A. Rynearson. 2014. Evolutionary potential of marine phytoplankton under ocean acidification. Evolutionary Applications 7:140–155, https://doi.org/10.1111/eva.12120.

Crawfurd, K.J., J.A. Raven, G.L. Wheeler, E.J. Baxter, and I. Joint. 2011. The response of Thalassiosira pseudonana to long-term exposure to increased CO2 and decreased pH. PLoS ONE 6(10), https://doi.org/10.1371/journal.pone.0026695.

Crawley, A., D.I. Kline, S. Dunn, K. Anthony, and S. Dove. 2010. The effect of ocean acidification on symbiont photorespiration and productivity in Acropora Formosa. Global Change Biology 16(2):851–863, https://doi.org/10.1111/j.1365-2486.2009.01943.x.

Dason, J.S., E. Huertas, and B. Colman. 2004. Source of inorganic carbon for photosynthesis in two marine dinoflagellates. Journal of Phycology 40:285–292, https://doi.org/10.1111/j.1529-8817.2004.03123.x.

De Beer, D., and A.W.D. Larkum. 2001. Photosynthesis and calcification in the calcifying algae Halimeda discoidea studied with microsensors. Plant, Cell and Environment 24:1,209–1,217, https://doi.org/10.1046/j.1365-3040.2001.00772.x.

De Bodt, C., N. Van Oostende, J. Harlay, K. Sabbe, and L. Chou. 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 7:1,401–1,412, https://doi.org/10.5194/bg-7-1401-2010.

Duarte, C.M., and J. Cebrian. 1996. The fate of marine autotrophic production. Limnology and Oceanography 41:1,758–1,766, https://doi.org/10.4319/lo.1996.41.8.1758.

Eichner, M., B. Rost, and S.A. Kranz. 2014. Diversity of ocean acidification effects on marine N-2 fixers. Journal of Experimental Marine Biology and Ecology 457:199–207, https://doi.org/10.1016/j.jembe.2014.04.015.

Errera, R.M., S. Yvon-Lewis, J.D. Kessler, and L. Campbell. 2014. Responses of the dinoflagellate Karenia brevis to climate change: pCO2 and sea surface temperatures. Harmful Algae 37:110–116, https://doi.org/10.1016/j.hal.2014.05.012.

Fabricius, K.E., C. Langdon, S. Uthicke, C. Humphrey, S. Noonan, G. De’ath, R. Okazaki, N. Muehillehner, M.S. Glas, and J.M. Lough. 2011. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Climate Change 1:165–169, https://doi.org/10.1038/nclimate1122.

Falkowski, P.G., and J.A. Raven. 2007. Photosynthesis and primary production in nature. Chapter 9 in Aquatic Photosynthesis, 2nd ed. Princeton University Press, Princeton.

Feng, Y., M.E. Warner, Y. Zhang, J. Sun, F.X. Fu, J.M. Rose, and D.A. Hutchins. 2008. Interactive effects of increased pCO2, temperature and irradiance on the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae). European Journal of Phycology 43:87–98, https://doi.org/10.1080/09670260701664674.

Ferrier-Pagès, C., J.-P. Gattuso, S. Dallot, and J. Jaubert. 2000. Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata. Coral Reefs 19(2):103–113, https://doi.org/10.1007/s003380000078.

Fiorini, S., J.J. Middelburg, and J.P. Gattuso. 2011a. Effects of elevated CO2 partial pressure and temperature on the coccolithophore Syracosphaera pulchra. Aquatic Microbial Ecology 64:221–232, https://doi.org/10.3354/ame01520.

Fiorini, S., J.J. Middelburg, and J.P. Gattuso. 2011b. Testing the effects of elevated pCO2 on coccolithophores (Prymnesiophyceae): Comparison between haploid and diploid life stages. Journal of Phycology 47:1,281–1,291, https://doi.org/10.1111/j.1529-8817.2011.01080.x.

Fu, F.-X., M.R. Mulholland, N.S. Garcia, A. Beck, P.W. Bernhardt, M.E. Warner, S.A. Sanudo-Wilhelmy, and D.A. Hutchins. 2008. Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera. Limnology and Oceanography 53:2,472–2,484, https://doi.org/10.4319/lo.2008.53.6.2472.

Fu, F.-X., A.R. Place, N.S. Garcia, and D.A. Hutchins. 2010. CO2 and phosphate availability control the toxicity of the harmful bloom dinoflagellate Karlodinium veneficum. Aquatic Microbial Ecology 59:55–65, https://doi.org/10.3354/ame01396.

Fu, F.-X., M.E. Warner, Y.H. Zhang, Y.Y. Feng, and D.A. Hutchins. 2007. Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). Journal of Phycology 43:485–496, https://doi.org/10.1111/j.1529-8817.2007.00355.x.

Garcia, N.S., F.X. Fu, C.L. Breene, P.W. Bernhardt, M.R. Mulholland, J.A. Sohm, and D.A. Hutchins. 2011. Interactive effects of irradiance and CO2 on CO2 fixation and N2 fixation in the diazotroph Trichodesmium erythraeum (Cyanobacteria). Journal of Phycology 47:1,292–1,303, https://doi.org/10.1111/j.1529-8817.2011.01078.x.

Garcia, N.S., F.-X. Fu, C.L. Breene, E.K. Yu, P.W. Bernhardt, M.R. Mulholland, and D.A. Hutchins. 2013a. Combined effects of CO2 and light on large and small isolates of the unicellular N2-fixing cyanobacterium Crocosphaera watsonii from the western tropical Atlantic Ocean. European Journal of Phycology 48:128–139, https://doi.org/10.1080/09670262.2013.773383.

Garcia, N.S., F.-X. Fu, and D.A. Hutchins. 2013b. Colimitation of the unicellular photosynthetic diazotroph Crocosphaera watsonii by phosphorus, light, and carbon dioxide. Limnology and Oceanography 58:1,501–1,512.

Giordano, M., J. Beardall, and J.A. Raven. 2005. CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology 56:99–131, https://doi.org/10.1146/annurev.arplant.56.032604.144052.

Gonzales, A.D., Y.K. Light, Z.D. Zhang, T. Iqbal, T.W. Lane, and A. Martino. 2005. Proteomic analysis of the CO2-concentrating mechanism in the open-ocean cyanobacterium Synechococcus WH8102. Canadian Journal of Botany 83:735–745, https://doi.org/10.1139/b05-056.

Gradoville, M.R., A.E. White, and R.M. Letelier. 2014. Physiological response of Crocosphaera watsonii to enhanced and fluctuating carbon dioxide conditions. PloS ONE 9(10), e110660, https://doi.org/10.1371/journal.pone.0110660.

Granum, E., J.A. Raven, and R.C. Leegood. 2005. How do marine diatoms fix 10 billion tonnes of inorganic carbon per year? Canadian Journal of Botany 83:898–908, https://doi.org/10.1139/b05-077.

Haimovich-Dayan, M., N. Garfinkel, D. Ewe, Y. Marcus, A. Gruber, H. Wagner, P.G. Kroth, and A. Kaplan. 2013. The role of C4 metabolism in the marine diatom Phaeodactylum tricornutum. New Phytologist 197:177–185, https://doi.org/10.1111/j.1469-8137.2012.04375.x.

Hare, C.E., K. Leblanc, G.R. DiTullio, R.M. Kudela, Y. Zhang, P.A. Lee, S. Riseman, and D.A. Hutchins. 2007. Consequences of increased temperature and CO2 for phytoplankton community structure in the Bering Sea. Marine Ecology Progress Series 352:9–16, https://doi.org/10.3354/meps07182.

Hoogstraten, A., K.R. Timmermans, and H.J.W. de Baar. 2012. Morphological and physiological effects in Proboscia alata (Bacillariophyceae) grown under different light and CO2 conditions of the modern Southern Ocean. Journal of Phycology 48:559–568, https://doi.org/10.1111/j.1529-8817.2012.01148.x.

Hopkinson, B.M., C.L. Dupont, A.E. Allen, and F.M.M. Morel. 2011. Efficiency of the CO2-concentrating mechanism of diatoms. Proceedings of the National Academy of Sciences of the United States of America 108:3,830–3,837, https://doi.org/10.1073/pnas.1018062108.

Hoppe, C.J.M., C.S. Hassler, C.D. Payne, P.D. Tortell, B. Rost, and S. Trimborn. 2013. Iron limitation modulates ocean acidification effects on Southern Ocean phytoplankton communities. PLoS ONE 8(11):e79890, https://doi.org/10.1371/journal.pone.0079890.

Hutchins, D.A., F.-X. Fu, E.A. Webb, N. Walworth, and A. Tagliabue. 2013. Taxon-specific response of marine nitrogen fixers to elevated carbon dioxide concentrations. Nature Geoscience 6:790–795, https://doi.org/10.1038/ngeo1858.

Hutchins, D.A., F.-X. Fu, Y. Zhang, M.E. Warner, Y. Feng, K. Portune, P.W. Bernhardt, and M.R. Mulholland. 2007. CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates and elemental ratios: Implications for past, present and future ocean biogeochemistry. Limnology and Oceanography 552:1,293–1,304, https://doi.org/10.4319/lo.2007.52.4.1293.

Iglesias-Rodriguez, M.D., P.R. Halloran, R.E.M. Rickaby, I.R. Hall, E. Colmenero-Hidalgo, J.R. Gittins, D.R.H. Green, T. Tyrrell, S.J. Gibbs, P. von Dassow, and others. 2008. Phytoplankton calcification in a high-CO2 world. Science 320:336–340, https://doi.org/10.1126/science.1154122.

Jacquet, S., M. Heldal, D. Iglesias-Rodriguez, A. Larsen, W. Wilson, and G. Bratbak. 2002. Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection. Aquatic Microbial Ecology 27:111–124, https://doi.org/10.3354/ame027111.

Johnson, V.R., C. Brownlee, R.E.M. Rickaby, M. Graziano, M. Milazzo, and J.M. Hall-Spencer. 2013. Responses of marine benthic microalgae to elevated CO2. Marine Biology 160:1,813–1,824, https://doi.org/10.1007/s00227-011-1840-2.

Kim, J.M., K. Lee, K. Shin, J.H. Kang, H.W. Lee, M. Kim, P.G. Jang, and M.C. Jang. 2006. The effect of seawater CO2 concentration on growth of a natural phytoplankton assemblage in a controlled mesocosm experiment. Limnology and Oceanography 51:1,629–1,636, https://doi.org/10.4319/lo.2006.51.4.1629.

Kirkham, A.R., C. Lepere, L.E. Jardillier, F. Not, H. Bouman, A. Mead, and D.J. Scanlan. 2013. A global perspective on marine photosynthetic picoeukaryote community structure. ISME Journal 7:922–936, https://doi.org/10.1038/ismej.2012.166.

Kleypas, J.A., R.A. Feely, V.J. Fabry, C. Langdon, C.L. Sabine, and L.L. Robbins. 2006. Impacts of Ocean Acidification on Coral Reefs and Other Marine Calcifiers: A Guide for Future Research. Report of a workshop held April 18–20, 2005, St. Petersburg, FL, sponsored by NSF, NOAA, and the US Geological Survey, 88 pp.

Koch, M., G. Bowes, C. Ross, and X.-H. Zhang. 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology 19:103–132, https://doi.org/10.1111/j.1365-2486.2012.02791.x.

Kranz, S.A., M. Eichner, and B. Rost. 2011. Interactions between CCM and N2 fixation in Trichodesmium. Photosynthesis Research 109:73–84, https://doi.org/10.1007/s11120-010-9611-3.

Kranz, S.A., O. Levitan, K.-U. Richter, O. Prasil, I. Berman-Frank, and B. Rost. 2010. Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: Physiological responses. Plant Physiology 154:334–345, https://doi.org/10.1104/pp.110.159145.

Kranz, S.A., D. Sültemeyer, K.-U. Richter, and B. Rost. 2009. Carbon acquisition in Trichodesmium: The effect of pCO2 and diurnal changes. Limnology and Oceanography 54:548–559, https://doi.org/10.4319/lo.2009.54.2.0548.

Kroth, P.G., A. Chiovitti, A. Gruber, V. Martin-Jezequel, T. Mock, M.S. Parker, M.S. Stanley, A. Kaplan, L. Caron, T. Weber, and others. 2008. A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS ONE 3(1):e1426, https://doi.org/10.1371/journal.pone.0001426.

Küpper, H., N. Ferimazova, I. Setlik, and I. Berman-Frank. 2004. Traffic lights in Trichodesmium: Regulation of photosynthesis for nitrogen fixation studied by chlorophyll fluorescence kinetic microscopy. Acta Physiologiae Plantarum 26:94–95, https://doi.org/10.1104/pp.104.045963.

Kustka, A.B., A.J. Milligan, H. Zheng, A.M. New, C. Gates, K.D. Bidle, and J.R. Reinfelder. 2014. Low CO2 results in a rearrangement of carbon metabolism to support C4 photosynthetic carbon assimilation in Thalassiosira pseudonana. New Phytologist 204:507–520, https://doi.org/10.1111/nph.12926.

Langdon, C., and M.J. Atkinson. 2005. Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. Journal of Geophysical Research 110, C09S07, https://doi.org/10.1029/2004JC002576.

Langer, G., M. Geisen, K.H. Baumann, J. Klas, U. Riebesell, S. Thoms, and J.R. Young. 2006. Species-specific responses of calcifying algae to changing seawater carbonate chemistry. Geochemistry Geophysics Geosystems 7, Q09006, https://doi.org/10.1029/2005GC001227.

Langer, G., G. Nehrke, I. Probert, J. Ly, and P. Ziveri. 2009. Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6:2,637–2,646, https://doi.org/10.5194/bg-6-2637-2009.

Langer, G. 2011. CO2 mediation of adverse effects of seawater acidification in Calcidiscus leptoporus. Geochemistry Geophysics Geosystems 12, Q05001, https://doi.org/10.1029/2010GC003393.

Law, C.S., E. Breitbarth, L.J. Hoffmann, C.M. McGraw, R.J. Langlois, J. LaRoche, A. Marriner, and K.A. Safi. 2012. No stimulation of nitrogen fixation by non-filamentous diazotrophs under elevated CO2 in the South Pacific. Global Change Biology 18:3,004–3,014, https://doi.org/10.1111/j.1365-2486.2012.02777.x.

Lefebvre, S.C., I. Benner, J.H. Stillman, A.E. Parker, M.K. Drake, P.E. Rossignol, K.M. Okimura, T. Komada, and E.J. Carpenter. 2012. Nitrogen source and pCO2 synergistically affect carbon allocation, growth and morphology of the coccolithophore Emiliania huxleyi: Potential implications of ocean acidification for the carbon cycle. Global Change Biology 18:493–503, https://doi.org/10.1111/j.1365-2486.2011.02575.x.

Leggat, W., M.R. Badger, and D. Yellowlees. 1999. Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiology 121(4):1,247–1,255, https://doi.org/10.1104/pp.121.4.1247.

Levitan, O., S.A. Kranz, D. Spungin, O. Prasil, B. Rost, and I. Berman-Frank. 2010a. Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: A mechanistic view. Plant Physiology 154:346–356, https://doi.org/10.1104/pp.110.159285.

Levitan, O., G. Rosenberg, I. Setlik, E. Setlikova, J. Grigel, J. Klepetar, O. Prasil, and I. Berman-Frank. 2007. Elevated CO2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Global Change Biology 13:531–538, https://doi.org/10.1111/j.1365-2486.2006.01314.x.

Levitan, O., S. Sudhaus, J. LaRoche, and I. Berman-Frank. 2010b. The influence of pCO2 and temperature on gene expression of carbon and nitrogen pathways in Trichodesmium IMS101. PLoS ONE 5(12), https://doi.org/10.1371/journal.pone.0015104.

Li, Y.H., J.T. Xu, and K.S. Gao. 2014. Light-modulated responses of growth and photosynthetic performance to ocean acidification in the model diatom Phaeodactylum tricornutum. PLoS ONE 9(5), https://doi.org/10.1371/journal.pone.0096173.

Liu, H., H.A. Nolla, and L. Campbell. 1997. Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquatic Microbial Ecology 12:39–47, https://doi.org/10.1029/1998JC900011.

Lohbeck, K.T., U. Riebesell, and T.B.H. Reusch. 2012. Adaptive evolution of a key phytoplankton species to ocean acidification. Nature Geoscience 5:346–351, https://doi.org/10.1038/ngeo1441.

Lomas, M.A., B.M. Hopkinson, J.L. Losh, D.E. Ryan, D.L. Shi, Y. Xu, and F.M.M. Morel. 2012. Effect of ocean acidification on cyanobacteria in the subtropical North Atlantic. Aquatic Microbial Ecology 66:211–222, https://doi.org/10.3354/ame01576.

Losh, J.L., J.N. Young, and F.M. Morel. 2013. Rubisco is a small fraction of total protein in marine phytoplankton. New Phytologist 198:52–58, https://doi.org/10.1111/nph.12143.

Lundholm, N., P.J. Hansen, and Y. Kotaki. 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, https://doi.org/10.3354/meps273001.

Luo, Y.W., S.C. Doney, L.A. Anderson, M. Benavides, A. Bode, S. Bonnet, K.H. Boström, D. Böttjer, D.G. Capone, E.J. Carpenter, and others. 2012. Database of diazotrophs in global ocean: Abundances, biomass and nitrogen fixation rates. Earth System Science Data Discussion 5(1):47–106, https://doi.org/10.5194/essd-4-47-2012.

Mackey, K.R.M., A. Paytan, K. Caldiera, A. Grossman, D. Moran, M. McIlvin, and M. Saito. 2013. Effect of temperature on photosynthesis and growth in marine Synechococcus. Plant Physiology 163:815–829, https://doi.org/10.1104/pp.113.221937.

Marubini, F., C. Ferrier-Pagès, P. Furla, and D. Allemand. 2008. Coral calcification responds to seawater acidification: A working hypothesis towards a physiological mechanism. Coral Reefs 27:491–99, https://doi.org/10.1007/s00338-008-0375-6.

Matsuda, Y., T. Hara, and B. Colman. 2011. Regulation of the induction of bicarbonate uptake by dissolved CO2 in the marine alga Phaeodactylum tricornutum. Plant, Cell & Environment 24:611–620, https://doi.org/10.1046/j.1365-3040.2001.00702.x.

Matsuda, Y., and P.G. Kroth. 2014. Carbon fixation in diatoms. Pp. 335–362 in Structural Basis of Biological Energy Generation. Advances in Photosynthesis and Respiration, vol. 39, https://doi.org/10.1007/978-94-017-8742-0_18.

Matsuda, Y., K. Nakajima, and M. Tachibana. 2011. Recent progresses on the genetic basis of the regulation of CO2 acquisition systems in response to CO2 concentration. Photosynthesis Research 109:191–203, https://doi.org/10.1007/s11120-011-9623-7.

McGinn, P.J., and F.M. Morel. 2008. Expression and regulation of carbonic anhydrases in the marine diatom Thalassiosira pseudonana and in natural phytoplankton assemblages from Great Bay, New Jersey. Physiologia Plantarum 133:78–91, https://doi.org/10.1111/j.1399-3054.2007.01039.x.

Milligan, A.J., I. Berman-Frank, Y. Gerchman, G.C. Dismukes, and P.G. Falkowski. 2007. Light-dependent oxygen consumption in nitrogen-fixing cyanobacteria plays a key role in nitrogenase protection. Journal of Phycology 43:845–852, https://doi.org/10.1111/j.1529-8817.2007.00395.x.

Mohr, W., M.P. Intermaggio, and J. LaRoche. 2010. Diel rhythm of nitrogen and carbon metabolism in the unicellular, diazotrophic cyanobacterium Crocosphaera watsonii WH8501. Environmental Microbiology 12:412–421, https://doi.org/10.1111/j.1462-2920.2009.02078.x.

Moisander, P.H., R.A. Beinart, I. Hewson, A.E. White, K.S. Johnson, C.A. Carlson, J.P. Montoya, and J.P. Zehr. 2010. Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science 327:1,512–1,514, https://doi.org/10.1126/science.1185468.

Morel, F.M.M. 1987. Kinetics of nutrient uptake and growth in phytoplankton. Journal of Phycology 23:137–150, https://doi.org/10.1111/j.1529-8817.1987.tb04436.x.

Morel, F.M.M., E.H. Cox, A.M.L. Kraepiel, T.W. Lane, A.J. Milligan, I. Schaperdoth, J.R. Reinfelder, and P.D. Tortell. 2002. Acquisition of inorganic carbon by the marine diatom Thalassiosira weissflogii. Functional Plant Biology 29:301–308, https://doi.org/10.1071/PP01199.

Morris, J.J., and E.R. Zinser. 2013. Continuous hydrogen peroxide production by organic buffers in phytoplankton culture media. Journal of Phycology 49:1,223–1,228, https://doi.org/10.1111/jpy.12123.

Müller, M.N., L. Beaufort, O. Bernard, M.L. Pedrotti, A. Talec, and A. Sciandra. 2012. Influence of CO2 and nitrogen limitation on the coccolith volume of Emiliania huxleyi (Haptophyta). Biogeosciences 9:4,155–4,167, https://doi.org/10.5194/bg-9-4155-2012.

Müller, M.N., K.G. Schulz, and U. Riebesell. 2010. Effects of long-term high CO2 exposure on two species of coccolithophores. Biogeosciences 7:1,109–1,116.

Nelson, D.M., P. Tréguer, M.A. Brzezinski, A. Leynaert, and B. Quéginer. 1995. Production and dissolution of biogenic silica in the ocean: Revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochemical Cycles 9:359–372, https://doi.org/10.1029/95GB01070.

Nelson, W.A. 2009. Calcified macroalgae—critical to coastal ecosystems and vulnerable to change: A review. Marine and Freshwater Research 60:787–801, https://doi.org/10.1071/MF08335.

Nimer, N.A., C. Brownlee, and M.J. Merrett. 1999. Extracellular carbonic anhydrase facilitates carbon dioxide availability for photosynthesis in the marine dinoflagellate Prorocentrum micans. Plant Physiology 120(1):105–11.

Orr, J.C., V.J. Fabry, O. Aumont, L. Bopp, S.C. Doney, R.A. Feely, A. Gnanadesikan, N. Gruber, A. Ishida, F. Joos, and others. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686, https://doi.org/10.1038/nature04095.

Pan, Y.L., D.V.S. Rao, and K.H. Mann. 1996. Changes in domoic acid production and cellular chemical composition of the toxigenic diatom Pseudo-nitzschia multiseries under phosphate limitation. Journal of Phycology 32:371–381, https://doi.org/10.1111/j.0022-3646.1996.00371.x.

Paulino, A.I., J.K. Egge, and A. Larsen. 2008. Effects of increased atmospheric CO2 on small and intermediate sized osmotrophs during a nutrient induced phytoplankton bloom. Biogeosciences 5:739–748, https://doi.org/10.5194/bg-5-739-2008.

Porzio, L., M.C. Buia, and J.M. Hall-Spencer. 2011. Effects of ocean acidification on macroalgal communities. Journal of Experimental Marine Biology and Ecology 400:278–287, https://doi.org/10.1016/j.jembe.2011.02.011.

Price, G.D., M.R. Badger, F.J. Woodger, and B.M. Long. 2008. Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): Functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. Journal of Experimental Botany 59:1,441–1,461, https://doi.org/10.1093/jxb/erm112.

Price, G.D., and M.R. Badger. 1989. Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC7942 creates a high CO2-requiring phenotype: Evidence for a central role for carboxysomes in the CO2 concentrating mechanism. Plant Physiology 91:505–513, https://doi.org/10.1104/pp.91.2.505.

Price, G.D., J.R. Coleman, and M.R. Badger. 1992. Association of carbonic anhydrase activity with carboxysomes isolated from the cyanobacterium Synechococcus PCC7942. Plant Physiology 100:784–793, https://doi.org/10.1104/pp.100.2.784.

Ramos, J.B.E., M.N. Müller, and U. Riebesell. 2010. Short-term response of the coccolithophore Emiliania huxleyi to an abrupt change in seawater carbon dioxide concentrations. Biogeosciences 7:177–186.

Ratti, S., M. Giordano, and D. Morse. 2007. CO2-concentrating mechanisms of the potentially toxic dinoflagellate Protoceratium reticulatum (Dinophyceae, Gonyaulacales). Journal of Phycology 43:693–701, https://doi.org/10.1111/j.1529-8817.2007.00368.x.

Raven, J.A., J. Beardall, and M. Giordano. 2014. Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms. Photosynthesis Research 121:111–124, https://doi.org/10.1007/s11120-013-9962-7.

Raven, J.A. 1997. Inorganic carbon acquisition by marine autotrophs. Advances in Botanical Research 27:85–209, https://doi.org/10.1016/S0065-2296(08)60281-5.

Read, B.A., J. Kegel, M.J. Klute, A. Kuo, S.C. Lefebvre, F. Maumus, C. Mayer, J. Miller, A. Monier, A. Salamov, and others. 2013. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499:209–213, https://doi.org/10.1038/nature12221.

Reinfelder, J.R., A.M. Kraepiel, and F.M. Morel. 2000. Unicellular C4 photosynthesis in a marine diatom. Nature 407:996–999, https://doi.org/10.1038/35039612.

Reinfelder, J.R., A.J. Milligan, and F.M. Morel. 2004. The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiology 135:2,106–2,111, https://doi.org/10.1104/pp.104.041319.

Richier, S., S. Fiorini, M.E. Kerros, P. von Dassow, and J.P. Gattuso. 2011. Response of the calcifying coccolithophore Emiliania huxleyi to low pH/high pCO2: From physiology to molecular level. Marine Biology 158:551–560, https://doi.org/10.1007/s00227-010-1580-8.

Riebesell, U., J. Czerny, K. von Brockel, T. Boxhammer, J. Budenbender, M. Deckelnick, M. Fischer, D. Hoffmann, S.A. Krug, U. Lentz, and others. 2013. Technical note: A mobile sea-going mesocosm system—new opportunities for ocean change research. Biogeosciences 10:1,835–1,847, https://doi.org/10.5194/bg-10-1835-2013.

Riebesell, U., I. Zondervan, B. Rost, P.D. Tortell, R.E. Zeebe, and F.M.M. Morel. 2000. Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407:364–367, https://doi.org/10.1038/35030078.

Riebesell, U. 2004. Effects of CO2 enrichment on marine phytoplankton. Journal of Oceanography 60:719–729, https://doi.org/10.1007/s10872-004-5764-z.

Ritson-Williams, R., S.N. Arnold, N.D. Fogarty, R.S. Steneck, M.J.A. Vermeij, and V.J. Paul. 2009. New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithsonian Contributions to the Marine Sciences 38:437–457, https://doi.org/10.5479/si.01960768.38.437.

Roberts, K., E. Granum, R.C. Leegood, and J.A. Raven. 2007a. C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiology 145:230–235, https://doi.org/10.1104/pp.107.102616.

Roberts, K., E. Granum, R.C. Leegood, and J.A. Raven. 2007b. Carbon acquisition by diatoms. Photosynthesis Research 93:79–88, https://doi.org/10.1007/s11120-007-9172-2.

Rokitta, S.D., and B. Rost. 2012. Effects of CO2 and their modulation by light in the life-cycle stages of the coccolithophore Emiliania huxleyi. Limnology and Oceanography 57(2):607–618, https://doi.org/10.4319/lo.2012.57.2.0607.

Rost, B., R. K.-U. Richter, U. Riebesell, and P.J. Hansen. 2006. Inorganic carbon acquisition in red tide dinoflagellates. Plant, Cell & Environment 29:810–822, https://doi.org/10.1111/j.1365-3040.2005.01450.x.

Rost, B., U. Riebesell, S. Burkhardt, and D. Sueltemeyer. 2003. Carbon acquisition of bloom-forming marine phytoplankton. Limnology and Oceanography 48:55–67, https://doi.org/10.4319/lo.2003.48.1.0055.

Rost, B., I. Zondervan, and D. Wolf-Gladrow. 2008. Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: Current knowledge, contradictions and research directions. Marine Ecology Progress Series 373:227–237, https://doi.org/10.3354/meps07776.

Scanlan, D.J., M. Ostrowski, S. Mazard, A. Dufresne, L. Garczarek, W.R. Hess, A.F. Post, M. Hagemann, I. Paulsen, and F. Partensky. 2009. Ecological genomics of marine picocyanobacteria. Microbiology and Molecular Biology Reviews 73:249–299.

Schaum, E., B. Rost, A.J. Millar, and S. Collins. 2013. Variation in plastic responses of a globally distributed picoplankton species to ocean acidification. Nature Climate Change 3:298–302, https://doi.org/10.1038/nclimate1774.

Schwarz, A., M. Björk, T. Buluda, M. Mtolera, and S. Beer. 2000. Photosynthetic utilisation of carbon and light by two tropical seagrass species as measured in situ. Marine Biology 137:755–761, https://doi.org/10.1007/s002270000433.

Sherman, L.A., P. Meunier, and M.S. Colon-Lopez. 1998. Diurnal rhythms in metabolism: A day in the life of a unicellular, diazotrophic cyanobacterium. Photosynthesis Research 58:25–42, https://doi.org/10.1023/A:1006137605802.

Shi, D., Y. Xu, and F.M.M. Morel. 2009. Effects of the pH/pCO2 control method on medium chemistry and phytoplankton growth. Biogeosciences 6:1,199–1,207, https://doi.org/10.5194/bg-6-1199-2009.

Shi, D.L., S.A. Kranz, J.M. Kim, and F.M.M. Morel. 2012. Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions. Proceedings of the National Academy of Sciences of the United States of America 109:E3094–E3100, https://doi.org/10.1073/pnas.1216012109.

Sobrino, C., M.L. Ward, and P.J. Neale. 2008. Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: Effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnology and Oceanography 53:494–505, https://doi.org/10.4319/lo.2008.53.2.0494.

Spielmeyer, A., and G. Pohnert. 2012. Influence of temperature and elevated carbon dioxide on the production of dimethylsulfoniopropionate and glycine betaine by marine phytoplankton. Marine Environmental Research 73:62–69, https://doi.org/10.1016/j.marenvres.2011.11.002.

Spungin, D., I. Berman-Frank, and O. Levitan. 2014. Trichodesmium’s strategies to alleviate phosphorus limitation in the future acidified oceans. Environmental Microbiology 16:1,935–1,947, https://doi.org/10.1111/1462-2920.12424.

Sun, J., D.A. Hutchins, Y.Y. Feng, E.L. Seubert, D.A. Caron, and F.-X. Fu. 2011. Effects of changing pCO2 and phosphate availability on domoic acid production and physiology of the marine harmful bloom diatom Pseudo-nitzschia multiseries. Limnology and Oceanography 56:829–840, https://doi.org/10.4319/lo.2011.56.3.0829.

Tatters, A.O., L.J. Flewelling, F.-X. Fu, A.A. Granholm, and D.A. Hutchins. 2013a. High CO2 promotes the production of paralytic shellfish poisoning toxins by Alexandrium catenella from Southern California waters. Harmful Algae 30:37–43, https://doi.org/10.1016/j.hal.2013.08.007.

Tatters, A.O., F.-X. Fu, and D.A. Hutchins. 2012. High CO2 and silicate limitation synergistically increase the toxicity of Pseudo-nitzshia fraudulenta. PLoS ONE 7(2), e32116, https://doi.org/10.1371/journal.pone.0032116.

Tatters, A.O., M.Y. Roleda, A. Schnetzer, F.-X. Fu, C.L. Hurd, P.W. Boyd, D.A. Caron, A.A.Y. Lie, L.J. Hoffmann, and D.A. Hutchins. 2013b. Short- and long-term conditioning of a temperate marine diatom community to acidification and warming. Philosophical Transactions of the Royal Society B 368, https://doi.org/10.1098/rstb.2012.0437.

Tchernov, D., J. Silverman, B. Luz, L. Reinhold, and A. Kaplan. 2003. Massive light-dependent cycling of inorganic carbon between oxygenic photosynthetic microorganisms and their surroundings. Photosynthesis Research 77:95–103, https://doi.org/10.1023/A:1025869600935.

Thompson, R.C., T.A. Norton, and S.J. Hawkins. 2004. Physical stress and biological control regulate the producer-consumer balance in intertidal biofilms. Ecology 85:1,372–1,382, https://doi.org/10.1890/03-0279.

Traving, S.J., M.R.J. Clokie, and M. Middelboe. 2013. Increased acidification has a profound effect on the interactions between the cyanobacterium Synechococcus sp. WH7803 and its viruses. FEMS Microbiology Ecology 87:133–141, https://doi.org/10.1111/1574-6941.12199.

Tortell, P.D., G.R. DiTullio, D.M. Sigman, and F.M.M. Morel. 2002. CO2 effects on taxonomic composition and nutrient utilization in an equatorial Pacific phytoplankton assemblage. Marine Ecology Progress Series 236:37–43, https://doi.org/10.3354/meps236037.

Tortell, P.D., C.D. Payne, Y.Y. Li, S. Trimborn, B. Rost, W.O. Smith, C. Riesselman, R.B. Dunbar, P. Sedwick, and G.R. DiTullio. 2008. CO2 sensitivity of Southern Ocean phytoplankton. Geophysical Research Letters 35, L04605, https://doi.org/10.1029/2007gl032583.

Tortell, P.D. 2000. Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnology and Oceanography 45:744–750, https://doi.org/10.4319/lo.2000.45.3.0744.

Trimborn, S., T. Brenneis, E. Sweet, and B. Rost. 2013. Sensitivity of Antarctic phytoplankton species to ocean acidification: Growth, carbon acquisition, and species interaction. Limnology and Oceanography 58:997–1,007, https://doi.org/10.4319/lo.2013.58.3.0997.

Trimborn, S., N. Lundholm, S. Thoms, K.-U. Richter, B. Krock, P.J. Hansen, and B. Rost. 2008. Inorganic carbon acquisition in potentially toxic and non-toxic diatoms: The effect of pH-induced changes in seawater carbonate chemistry. Physiologia Plantarum 133:92–105, https://doi.org/10.1111/j.1399-3054.2007.01038.x.

Trimborn, S., D. Wolf-Gladrow, and K.-U. Richter, and B. Rost. 2009. The effect of pCO2 on carbon acquisition and intracellular assimilation in four marine diatom species. Journal of Experimental Marine Biology and Ecology 376:26–36, https://doi.org/10.1016/j.jembe.2009.05.017.

Underwood, A.J. 1984. The vertical-distribution and seasonal abundance of intertidal microalgae on a rocky shore in New South Wales. Journal of Experimental Marine Biology and Ecology 78:199–220, https://doi.org/10.1016/0022-0981(84)90159-X.

Wannicke, N., S. Endres, A. Engel, H.P. Grossart, M. Nausch, J. Unger, and M. Voss. 2012. Response of Nodularia spumigena to pCO2: Part 1. Growth, production and nitrogen cycling.

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