Oceanography The Official Magazine of
The Oceanography Society
Volume 22 Issue 04

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Volume 22, No. 4
December 2009

Nutrient Cycles and Marine Microbes in a CO2-Enriched Ocean

David A. Hutchins | Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA
Margaret R. Mulholland | Department of Ocean, Earth, and Atmospheric Sciences, Old Dominion University, Norfolk, VA, USA
Feixue Fu | Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA

Article Abstract

The ocean carbon cycle is tightly linked with the cycles of the major nutrient elements nitrogen, phosphorus, and silicon. It is therefore likely that enrichment of the ocean with anthropogenic CO2 and attendant acidification will have large consequences for marine nutrient biogeochemistry, and for the microbes that mediate many key nutrient transformations. The best available evidence suggests that the nitrogen cycle may respond strongly to higher CO2 through increases in global N2 fixation and possibly denitrification, as well as potential decreases in nitrification. These trends could cause nitrification to become a nitrogen cycle “bottleneck,” by increasing the flux of N2 fixed into ammonium while decreasing the fraction being oxidized to nitrite and nitrate. The consequences could include reduced supplies of oxidized nitrogen substrates to denitrifiers, lower levels of nitrate-supported new primary production, and expansion of the regenerated production system accompanied by shifts in current phytoplankton communities. The phosphorus and silicon cycles seem less likely to be directly affected by enhanced CO2 conditions, but will undoubtedly respond indirectly to changing carbon and nitrogen biogeochemistry. A review of culture experiments that examined the effects of increased CO2 on elemental ratios of phytoplankton suggests that for most cyanobacteria and eukaryotes, C:N and N:P ratios will either remain at Redfield values or increase substantially. Natural plankton community CO2 manipulation experiments show much more mixed outcomes, with both increases and decreases in C:N and N:P ratios reported at future CO2 levels. We conclude our review with projections of overall trends in the cycles of nitrogen, phosphorus, and silicon over the next century as they respond to the steady accumulation of fossil-fuel-derived CO2 in a rapidly changing ocean.

Citation

Hutchins, D.A., M.R. Mulholland, and F. Fu. 2009. Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22(4):128–145, http://dx.doi.org/10.5670/oceanog.2009.103.

References

Altabet, M.A., M.J. Higginson, and D.W. Murray. 2002. The effect of millennial-scale changes in Arabian Sea denitrification on atmospheric CO2. Nature 415:159–162.

Bange, H.W. 2008. Gaseous nitrogen compounds (NO, N2O, N2, NH3) in the ocean. Pp. 51–94 in Nitrogen in the Marine Environment, 2nd ed. D.G. Capone, D.A. Bronk, M.R. Mulholland, and E.J. Carpenter, eds, Elsevier Press, Amsterdam.

Barcelos e Ramos, J.B.E., 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, doi:10.1029/2006GB002898.

Bellerby, R.G.J., K.G. Schulz, U. Riebesell, C. Neill, G. Nondal, E. Heegaard, T. Johannessen, and K.R. Brown. 2008. Marine ecosystem community carbon and nutrient uptake stoichiometry under varying ocean acidification during the PeECE III experiment. Biogeosciences 5:1,517–1,527.

Beman, J.M., C.E. Chow, B.N. Popp, J.A. Fuhrman, Y. Feng, and D.A. Hutchins. 2008. Alteration of oceanic nitrification under elevated carbon dioxide concentrations. Paper presented at ASLO meeting, Nice, France, January 25–30, 2008. Abstract available online at: http://www.sgmeet.com/aslo/nice2009/viewabstract2.asp?AbstractID=5886 (accessed November 17, 2009).

Blackford, J.C., and F.J. Gilbert. 2007. pH variability and CO2 induced acidification in the North Sea. Journal of Marine Systems 64:229–241.

Boyd, P.W., R. Strzepek, R., F.-X. Fu, and D.A. Hutchins. In press. Environmental control of open ocean phytoplankton groups: Now and in the future. Limnology and Oceanography.

Burkhardt, S., I. Zondervan, and U. Riebesell. 1999. Effect of CO2 concentration on C:N:P ratio in marine phytoplankton: A species comparison. Limnology and Oceanography 44(3):683–690.

Carpenter, E.J., and D.G. Capone. 2008. Nitrogen fixation. Pp. 141–198 in Nitrogen in the Marine Environment, 2nd ed. D.G. Capone, D.A. Bronk, M.R. Mulholland, and E.J. Carpenter, eds, Elsevier Press, Amsterdam.

Collins, S., and G. Bell. 2006. Evolution of natural algal populations at elevated CO2. Ecological Letters 9:129–135.

Czerny, J., J. Barcelos e Ramos, and U. Riebesell. 2009. Influence of elevated CO2 concentrations on cell division and nitrogen fixation rates in the bloom-forming cyanobacterium Nodularia spumigena. Biogeosciences 6:1,865–1,875.

Devol, A.H. 2008. Denitrification including anammox. Pp. 263–302 in Nitrogen in the Marine Environment, 2nd ed. D.G. Capone, D.A. Bronk, M.R. Mulholland, and E.J. Carpenter, eds, Elsevier Press, Amsterdam.

Engel, A., I. Zondervan, K. Aerts, L. Beaufort, A. Benthien, L. Chou, B. Delille, J.-P. Gattuso, J. Harlay, C. Heemann, and others. 2005. Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments. Limnology and Oceanography 50(2):493–507.

Fabry, V.J., C. Langdon, W.M. Balch, A.G. Dickson, R.A. Feely, B. Hales, D.A. Hutchins, J.A. Kleypas, and C.L. Sabine. 2008. Ocean acidification’s effects on marine ecosystems and biogeochemistry. Eos, Transactions, American Geophysical Union 89:143–144.

Feely, R.A., C.L. Sabine, K. Lee, W. Berelson, J. Kleypas, V.J. Fabry, and F.J. Millero. 2004. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366.

Feng, Y., W.E. Warner, Y. Zhang, J. Sun, F.-X. Fu, 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, doi:10.1080/09670260701664674.

Feng, Y., C.E. Hare, K. Leblanc, J. Rose, Y. Zhang, G.R. DiTullio, P.A. Lee, S.W. Wilhelm, J.M. Rowe, J. Sun, and others. 2009. The effects of increased pCO2 and temperature on the North Atlantic Spring Bloom. I. The phytoplankton community and biogeochemical response. Marine Ecology Progress Series 388:13–25.

Feng, Y., C.E. Hare, J.M. Rose, S.M. Handy, G.R. DiTullio, P.A. Lee, W.O. Smith Jr., J. Peloquin, S. Tozzi, J. Sun, and others. In Press. Interactive effects of iron, irradiance, and CO2 on Ross Sea phytoplankton. Deep-Sea Research Part I.

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

Fu, F.-X., M.E. Warner, Y. Zhang, Y. Feng, and D.A. Hutchins. 2007. Effects of increased temperature and CO2 on photosynthesis, growth and elemental ratios of marine Synechococcus and Prochlorococcus (Cyanobacteria). Journal of Phycology 43:485–496.

Fu, F.-X., Y. Zhang, M.E. Warner, Y. Feng, and D.A. Hutchins. 2008b. A comparison of future increased CO2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful Algae 7, doi:10.1016/
j.hal.2007.05.006.

Galloway, J.N., F.J. Dentener, D.G. Capone, E.W. Boyer, R.W. Howarth, S.P. Seitzinger, G.P. Asner, C.C. Cleveland, P.A. Green, E.A. Holland, and others. 2004. Nitrogen cycles: Past, present, and future. Biogeochemistry 70:153–226.

Gervais, F., and U. Riebesell. 2001. Effect of phosphorus limitation on elemental composition and stable carbon isotope fractionation in a marine diatom growing under different CO2 concentrations. Limnology and Oceanography 46(3):497–504.

Gnanadesikan, A., J.L. Russell, and F. Zang. 2007. How does the ocean ventilation change under global warming? Ocean Science 3:43–53.

Ghafari, S., M. Hasan, and M.K. Aroua. 2009. Effect of carbon dioxide and bicarbonate as inorganic carbon sources on growth and adaptation of autohydrogenotrophic denitrifying bacteria. Journal of Hazardous Materials 162:1,507–1,513.

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

Huesemann, M.H., A.D. Skillman, and E.A. Crecelius. 2002. The inhibition of marine nitrification by ocean disposal of carbon dioxide. Marine Pollution Bulletin 44:142–148.

Hutchins, D.A., and F.-X. Fu. 2008. Linking the oceanic biogeochemistry of iron and phosphorus with the marine nitrogen cycle. Pp. 1,627–1,653 in Nitrogen in the Marine Environment, 2nd ed. D.G. Capone, D.A. Bronk, M.R. Mulholland, and E.J. Carpenter, eds, Elsevier Press, Amsterdam.

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 52:1,293–1,304.

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(5874):336–340, doi:10.1126/science.1154122.

Kleypas, J.A., R.W. Buddemeier, D. Archer, J.-P. Gattuso, C. Langdon, and B.N. Opdyke. 1999. Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120.

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(4):1,629–1,636.

Kranz, S.A., D. Sültemeyer, K.-U. Richter, and B. Rost. 2009. Carbon acquisition by Trichodesmium: The effect of pCO2 and diurnal changes. 2009. Limnology and Oceanography 54(2):548–559.

Leonardos, N., and R.J. Geider. 2005. Elevated atmospheric carbon dioxide increases organic carbon fixation by Emiliania huxleyi (Haptophyta) under nutrient-limited high-light conditions. Journal of Phycology 41:1,196–1,203.

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.

Mahaffey, C., A.F. Michaels, and D.G. Capone. 2005. The conundrum of marine N2 fixation. American Journal of Science 305:546–595.

Mahowald, N.M., and C. Luo. 2003. A less dusty future? Geophysical Research Letters 30(17), 1903, doi:10.1029/2003GL017880.

Matear, R.J., and R.C. Hirst. 2003. Long-term changes in dissolved oxygen concentrations in the ocean caused by protracted global warming. Global Biogeochemical Cycles 17(4):1,125, doi:10.1029/2002GB001997.

Millero, F.J. 2007. The marine inorganic carbon cycle. Chemical Reviews 107:308–341.

Millero, F.J., R. Woosley, B. DiTrolio, and J. Waters. 2009. Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22(4):72–85.

Milligan, A.J., D.E. Varela, M.A. Brzezinski, and F.M.M. Morel. 2004. Dynamics of silicon metabolism and silicon isotopic discrimination in a marine diatom as a function of pCO2. Limnology and Oceanography 49(2):322–329.

Montoya, J.P., C.M. Holl, J.P. Zehr, A. Hansen, T.A. Villareal, and D.G. Capone. 2004. High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430:1,027–1,032.

Mulholland, M.R., and M.W. Lomas. 2008. Nitrogen uptake and assimilation. Pp. 303–385 in Nitrogen in the Marine Environment, 2nd ed. D.G. Capone, D.A. Bronk, M.R. Mulholland, and E.J. Carpenter, eds, Elsevier Press, Amsterdam.

Mulholland, M.R., and P.W. Bernhardt. 2005. The effect of growth rate, phosphorus concentration, and temperature on N2 fixation, carbon fixation, and nitrogen release in continuous cultures of Trichodesmium IMS101. Limnology and Oceanography 50:839–849.

Najjar, R.G., C.R. Pyke, M.B. Adams, D. Breitburg, M. Kemp, C. Hershner, R. Howarth, M. Mulholland, M. Paolisso, D. Secor, K. Sellner, D. Wardrop, and R. Wood. In press. Potential climate-change impacts on the Chesapeake Bay. Estuarine, Coastal, and Shelf Science.

Oschlies, A., K.G. Schulz, U. Riebesell, and A. Schmittner. 2008. Simulated 21st century’s increase in oceanic suboxia by CO2-enhanced biotic carbon export. Global Biogeochemical Cycles 22, GB4008, doi:10.1029/2007GB003147.

Prufert-Bebout, L., H.W. Paerl, and C. Lassen. 1993. Growth, nitrogen fixation, and spectral attenuation in cultivated Trichodesmium species. Applied and Environmental Microbiology 59:1,367–1,375.

Redfield, A.C. 1958. The biological control of chemical factors in the environment. American Scientist 46(3):205–221.

Riebesell, U. 2004. Effects of CO2 enrichment on marine phytoplankton. Journal of Oceanography 60(4):719–729.

Riebesell, U., K.G. Schulz, R.G.J. Bellerby, M. Botros, P. Fritsche, M. Meyerhofer, C. Neill, G. Nondal, A. Oschlies, J. Wohlers, and E. Zollner. 2007. Enhanced biological carbon consumption in a high CO2 ocean. Nature 450:545–548, doi:10.1038/nature06267.

Robinson, R.S., A. Mix, and P. Martinez. 2007. Southern Ocean control on the extent of denitrification in the southeast Pacific over the last 70 ky. Quaternary Science Review 26:2,001–2,212.

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.

The Royal Society. 2005. Ocean acidification due to increasing atmospheric carbon dioxide. Policy document 12/05 ISBN 0 85403 617 2. Abstract available online at: http://www.royalsoc.ac.uk/Report_WF.aspx?pageid=9633&terms=Ocean+
acidification+due+to+increasing+atmospheric+
carbon+dioxide (accessed November 17, 2009).

Saito, M.A., T.J. Goepfert, and J.T. Ritt. 2008. Some thoughts on the concept of colimitation: Three definitions and the importance of bioavailability. Limnology and Oceanography 53:276–290.

Sañudo-Wilhelmy, S.A., A.B. Kustka, C.J. Gobler, D.A. Hutchins, M. Yang, K. Lwiza, J. Burns, D.G. Capone, J.A. Raven, and E.J. Carpenter. 2001. Phosphorus limitation of nitrogen fixation by Trichodesmium in the central North Atlantic Ocean. Nature 411:66–69.

Sarmiento, J.L., T.M.C. Hughes, R.J. Stouffer, and S. Manabe. 1998. Simulated response of the ocean carbon cycle to anthropogenic climate warming. Nature 393:245–249, doi:10.1038/30455.

Sedwick, P.N., E.R. Sholkovitz, and T.M. Church. 2007. Impact of anthropogenic combustion emissions on the fractional solubility of aerosol iron: Evidence from the Sargasso Sea. Geochemistry Geophysics Geosystems 8, Q10Q06, doi:10.1029/2007GC001586.

Takeda, S., and A. Tsuda. 2005. An in situ iron-enrichment in the western subarctic Pacific (SEEDS): Introduction and summary. Progress in Oceanography 64:95–109.

Tanaka, T., T.F. Thingstad, T. Løvdal, H.-P. Grossart, A. Larsen, M. Allgaier, M. Meyerhofer, K.L. Schulz, J. Wohlers, E. Zollner, and U. Riebesell. 2008. Availability of phosphate for phytoplankton and bacteria and of glucose for bacteria at different pCO2 levels in a mesocosm study. Biogeosciences 5:669–678.

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.

Tortell, P.D., C.D. Payne, 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, doi:10.1029/2007GL032583.

Ward, B.B. 2008. Nitrification in marine systems. Pp. 199–262 in Nitrogen in the Marine Environment, 2nd ed. D.G. Capone, D.A. Bronk, M.R. Mulholland, and E.J. Carpenter, eds, Elsevier Press, Amsterdam.

Wu, J., W. Sunda, E.A. Boyle, and D.M. Karl. 2000. Phosphate depletion in the western North Atlantic Ocean. Science 289:759–762.

Yool, A., A.P. Martin, C. Fernandez, and D.R. Clark. 2007. The significance of nitrification for oceanic new production. Nature 447:1,000–1,002, doi:10.1038/nature05885.

Zehr, J.P., J.B. Waterbury, P.J. Turner, J.P. Montoya, E. Omoregie, G.F. Steward, A. Hansen, and D.M. Karl. 2001. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412:635–638.