Skip to main content Accesibility Help

Impact of low pH/high pCO2 on the physiological response and fatty acid content in diatom Skeletonema pseudocostatum

  • Bárbara G. Jacob (a1), Peter von Dassow (a2) (a3) (a4), Joe E. Salisbury (a5), Jorge M. Navarro (a6) (a7) and Cristian A. Vargas (a1) (a2) (a8)...

pCO2/pH perturbation experiments were carried out under two different pCO2 levels to evaluate effects of CO2-driven ocean acidification on semi-continuous cultures of the marine diatom Skeletonema pseudocostatum CSA48. Under higher pCO2/lowered pH conditions, our results showed that CO2-driven acidification had no significant impact on growth rate, chlorophyll-a, cellular abundance, gross photosynthesis, dark respiration, particulate organic carbon and particulate organic nitrogen between CO2-treatments, suggesting that S. pseudocostatum is adapted to tolerate changes of ~0.5 units of pH under high pCO2 conditions. However, dissolved organic carbon (DOC) concentration and DOC/POC ratio were significantly higher at high pCO2, indicating that a greater partitioning of organic carbon into the DOC pool was stimulated by high CO2/low pH conditions. Total fatty acids (FAs) were significantly higher under low pCO2 conditions. The composition of FAs changed from low to high pCO2, with an increase in the concentration of saturated and a reduction of monounsaturated FAs. Polyunsaturated FAs did not show significant differences between pCO2 treatments. Our results lead to the conclusion that the balance between negative or null effect on S. pseudocostatum ecophysiology upon low pH/high pCO2 conditions constitute an important factor to be considered in order to evaluate the global effect of rising atmospheric CO2 on primary productivity in coastal ocean. We found a significant decrease in total FAs, however no indications were found for a detrimental effect of ocean acidification on the nutritional quality in terms of essential fatty acids.

Corresponding author
Correspondence should be addressed to: B.G. Jacob, Department of Aquatic System, Aquatic Ecosystem Functioning Lab (LAFE), Faculty of Environmental Sciences & Environmental Sciences Center EULA Chile, Universidad de Concepción, Concepción 4070386, Chile email:
Hide All
Alldredge, A.L. and Jackson, G.A. (1995) Aggregation in marine systems. Deep-Sea Research II 42, 17.
Berge, T., Daugbjerg, N., Andersen, B.B. and Hansen, P.J. (2010) Effect of lowered pH on marine phytoplankton growth rates. Marine Ecology Progress Series 416, 7991.
Bermúdez, R., Feng, Y., Roleda, M.Y., Tatters, A.O., Hutchins, D.A., Larsen, T., Boyd, P.W., Hurd, C.L., Riebesell, U. and Winder, M. (2015) Long-term conditioning to elevated pCO2 and warming influences the fatty and amino acid composition of the diatom Cylindrotheca fusiformis . PLoS ONE 10, e0123945.
Boelen, P., Van de Poll, W.H., Van der Strate, H.J., Neven, I.A., Beardall, J. and Buma, A.G.J. (2011) Neither elevated nor reduced CO2 affects the photophysiological performance of the marine Antarctic diatom Chaetoceros brevis . Journal of Experimental Marine Biology and Ecology 406, 3845.
Borchard, C. and Engel, A. (2012) Organic matter exudation by Emiliania huxleyi under simulated future ocean conditions. Biogeosciences 9, 34053423.
Boyd, P.W., Strzepek, R., Fu, F. and Hutchins, D.A. (2010) Environmental control of open-ocean phytoplankton groups: now and in the future. Limnology and Oceanography 55, 13531376.
Burkhardt, S., Amoroso, G., Riebesell, U. and Sültemeyer, D. (2001) CO2 and HCO3 uptake in marine diatoms acclimated to different CO2 concentrations. Limnology and Oceanography 46, 13781391.
Burkhardt, S., Zondervan, I. and Riebesell, U. (1999) Effect of CO2 concentration on C:N:P ratio in marine phytoplankton: a species comparison. Limnology and Oceanography 44, 683690.
Caldeira, K. and Wickett, M.E. (2003) Anthropogenic carbon and ocean pH. Nature 425, 365.
Cao, Z., Dai, M., Zheng, N., Wang, D., Li, Q., Zhai, W., Meng, F. and Gan, J. (2011) Dynamics of the carbonate system in a large continental shelf system under the influence of both a river plume and coastal upwelling. Journal of Geophysical Research 116. doi: 10.1029/2010JG001596.
Carlson, C.A. (2002) Production and removal processes. In Hansell, D.A. and Carlson, C.A. (eds) Biogeochemistry of marine dissolved organic matter. San Diego, CA: Academic Press, pp. 91151.
Chen, X. and Gao, K. (2003) Effect of CO2 concentrations on the activity of photosynthetic CO2 fixation and extracellular carbonic anhydrase in the marine diatom Skeletonema costatum . Chinese Science Bulletin 48, 26162620.
Chen, X. and Gao, K. (2004) Photosynthetic utilisation of inorganic carbon and its regulation in the marine diatom Skeletonema costatum . Functional Plant Biology 31, 10271033.
Crawfurd, K.J., Raven, J.A., Wheeler, G.L., Baxter, E.J. and Joint, I. (2011) The response of Thalassiosira pseudonana to long-term exposure to increased CO2 and decreased pH. PLoS ONE 6, e26695.
Dickson, A.G. (1990) Standard potential of the reaction: AgCl(s) + ½ H2(g) = Ag(s) + HCl (aq), and the standard acidity constant of the ion HSO4 _ in synthetic seawater from 273.15 to 318.15 K. Journal of Chemical Thermodynamics 22, 113127.
Dickson, A.G., Afghan, J.D. and Anderson, G.C. (2003) Reference materials for oceanic CO2 analysis: a method for the certification of total alkalinity. Marine Chemistry 80, 185197.
Dickson, A.G. and Millero, F.J. (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Research 34, 17331743.
Di Martino, C., Delne, S., Alvino, A. and Loreto, F. (1999) Photorespiration rate in spinach leaves under moderate NaCl stress. Photosynthetica 36, 233242.
DOE (1994) Handbook of methods for the analysis of the various parameters of the carbon dioxide system in sea water; version 2. Dickson, A.G. and Goyet, C. (eds) ORNL/CDIAC-74. Available at
Downton, W.J.S. (1977) Photosynthesis in salt-stressed grapevines. Australian Journal of Plant Physiology 4, 183192.
Elzenga, J.T.M., Prins, H.B.A. and Stefels, J. (2000) The role of extracelular carbonic anhydrase activity in inorganic carbon utilization of Phaeocystis globosa (Prymnesiophyseae): a comparison with other marine algae using the isotopic disequilibrium technique. Limnology and Oceanography 45, 372380.
Engel, A. (2002) Direct relationship between CO2 uptake and transparent exopolymer particles production in natural phytoplankton. Journal of Plankton Research 24, 4953.
Engel, A., Borchard, C., Piontek, J., Schulz, K.G., Riebesell, U. and Bellerby, R. (2013) CO2 increases 14C primary production in an Arctic plankton community. Biogeosciences 10, 12911308.
Engel, A., Delill, B., Jacquet, S., Riebesell, U., Rochelle-Newall, E., Terbrüggen, A. and Zondervan, I. (2004) Transparent exopolymer particles and dissolved organic carbon production by Emiliania huxleyi exposed to different CO2 concentrations: a mesocosm experiment. Aquatic Microbial Ecology 34, 93104.
Feng, Y., Warner, M.E., Zhang, Y., Sun, J., Fu, F.X., Rose, J.M. and Hutchins, D.A. (2008) Interactive effects of increased pCO2, temperature and irradiance on the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae). European Journal Phycology 43, 8798.
Gao, K. and Campbell, D.A. (2014) Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review. Functional Plant Biology 41, 449459.
Gao, K., Helbling, E., Häder, D. and Hutchins, D.A. (2012) Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Marine Ecology Progress Series 470, 167189.
Gaarder, T. and Gran, H.H. (1927) Investigations of the production of plankton in the Oslo Fjord. Rapport et proce's verbaux du Conseil International pour l'Exploration de la Mer 42, 148.
Geider, R.J. and LaRoche, J. (2002) Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. European Journal of Phycology 37, 117.
Guillard, R.R.L. and Ryther, J.H. (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea . Cleve Canadian Journal of Microbiology 8, 229239.
Heber, U., Bligny, R., Streb, P. and Douce, R. (1996) Photorespiration is essential for the protection of the photosynthetic apparatus of C3 plants against photoinactivation under sunlight. Botanica Acta 109, 307315.
Hessen, D.O., Ågren, G.I. and Anderson, T.R. (2004) Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85, 11791192.
Hessen, D.O. and Anderson, T.R. (2008) Excess carbon in aquatic organisms and ecosystems: physiological, ecological and evolutionary implications. Limnology and Oceanography 53, 16851696.
Hofmann, D., Butler, J.H. and Tans, P.P. (2011) A new look at atmospheric carbon dioxide. Atmospheric Environment 43, 20842086.
Hopkinson, B.M., Meile, C. and Shen, C. (2013) Quantification of extracellular carbonic anhydrase activity in two marine diatoms and investigation of its role. Plant Physiology 162, 11421152.
Jiao, N., Herndl, G.J., Hansell, D.A., Benner, R., Kattner, G., Wilhelm, S.W., Kirchman, D.L., Weinhauer, M.G., Tingwei, L., Chen, F. and Azam, F. (2010) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nature Reviews Microbiology 8, 593599.
Jonasdottir, S.H., Trung, N.H., Hansen, F. and Gartner, S. (2005) Egg production and hatching success in the calanoid copepods Calanus helgolandicus and Calanus finmarchicus in the North Sea from March to September 2001. Journal of Plankton Research 27, 12391259.
Kattner, G. and Fricke, H.S.G. (1986) Simple gas-liquid chromatographic method for the simultaneous determination of fatty acids and alcohols in wax esters of marine organisms. Journal of Chromatography A 361, 263268.
Kim, J.M., Lee, K., Shin, K., Kang, J-H., Lee, H-W., Kim, M., Jang, P-G. and Jang, M.C. (2006) The effect of seawater CO2 concentration on growth of a natural phytoplankton assemblage in a controlled mesocosm experiment. Limnology and Oceanography 51, 16291636.
Kim, J.M., Lee, K., Shin, K., Yang, E.J., Engel, A., Karl, D.M. and Kim, H.C. (2011) Shifts in biogenic carbon flow from particulate to dissolved forms under high carbon dioxide and warm ocean conditions. Geophysical Research Letters 38, 15.
King, A.L., Jenkins, B.D., Wallace, J.R., Liu, Y., Wikfors, G.H., Milke, L.M. and Shannon, L.M. (2015) Effects of CO2 on growth rate, C:N:P, and fatty acid composition of seven marine phytoplankton species. Marine Ecology Progress Series 537, 5969.
King, A.L., Sañudo-Wilhelmy, S.A., Leblanc, K., Hutchins, D.A. and Fu, F. (2011) CO2 and vitamin B12 interactions determine bioactive trace metal requirements of a subarctic Pacific diatom. Multidisciplinary Journal of Microbial Ecology 5, 13881396.
Klein Breteler, W.C.M., Schogt, N. and Rampen, S. (2005) Effect of diatom nutrient limitation on copepod development: role of essential lipids. Marine Ecology Progress Series 291, 125133.
Laws, E.A. and Bannister, T.T. (1980) Nutrient- and light-limited growth of Thalassiosira fluviatilis in continuous culture, with implications for phytoplankton growth in the ocean. Limnology and Oceanography 25, 457473.
Li, W., Gao, K. and Beardall, J. (2012) Interactive effects of ocean acidification and nitrogen-limitation on the diatom Phaeodactylum tricornutum . PLoS ONE 7, e51590.
Li, Y.H., Xu, J.T. and Gao, K.S. (2014) Light-modulated responses of growth and photosynthetic performance to ocean acidification in the model diatom Phaeodactylum tricornutum . PLoS ONE 9. doi: 10.1371/journal.pone.0096173.
Leu, E., Daase, M., Schulz, K.G., Stuhr, A. and Riebesell, U. (2013) Effect of ocean acidification on the fatty acid composition of a natural plankton community. Biogeosciences 10, 11431153.
Lorenzen, C.J. (1966) A method for the continuous measurement of in vivo chlorophyll concentration. Deep Sea Research 13, 223227.
Low-Décarie, E., Fussmann, G.F. and Bell, G. (2011) The effect of elevated CO2 on growth and competition in experimental phytoplankton communities. Global Change Biology 17, 25252535.
Mackey, R.M., Morris, J.J., Morel, F.M.M. and Kranz, S.A. (2015) Response of photosynthesis to ocean acidification. Oceanography 28, 7491.
Mehrbach, C., Culberson, C., Hawley, J. and Pytkovicz, R. (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18, 897907.
Meinshausen, M., Smith, S.J., Calvin, K., Daniel, J.S., Kainuma, M.L.T., Lamarque, J-F., Matsumoto, K., Montzka, S.A., Raper, S.C.B., Riahi, K., Thomson, A., Velders, G.J.M. and van Vuuren, D.P.P. (2011) The RCP greenhouse gas concentrations and their extensions from 1765 to 2300. Climatic Change 109, 213. doi: 10.1007/s10584-011-0156-z.
Müller-Navarra, D.C., Brett, M.T., Park, S., Chandra, S., Ballantyne, A.P., Zorita, E. and Goldman, C.R. (2004) Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes. Nature 427, 6972.
Nelson, D.M., Treguer, P., Brzezinski, M.A., Leynaert, A. and Queguiner, B. (1995) Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochemical Cycle 9, 359372.
Nimer, N.A., Warren, M. and Merrett, M.J. (1998) The regulation of photosynthetic rate and activation of extracelular carbonic anhydrase under CO2-limiting conditions in the marine diatom Skeletonema costatum . Plant, Cell and Environment 21, 805812.
Passow, U. (2002) Transparent exopolymer particles (TEP) in aquatic environment. Progress in Oceanography 55, 287333.
Pierrot, D.E., Lewis, E. and Wallace, D.W.R. (2006) MS Excel program developed for CO2 system calculations. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy. Available at
Riebesell, U., Schulz, K.G., Bellerby, R.G.J., Botros, M., Fritsche, P., Meyerhöfer, M., Neill, C., Nondal, G., Oschlies, A., Wohlers, J. and Zöllner, E. (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450, 545548.
Rossoll, D., Bermúdez, R., Hauss, H., Schulz, K.G., Riebesell, U., Sommer, U. and Winder, M. (2012) Ocean acidification-induced food quality deterioration constrains trophic transfer. PLoS ONE 7, e34737.
Rost, B., Riebesell, U., Burkhardt, S. and Sültemeyer, D. (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnology and Oceanography 48, 5567.
Shamberger, K.E.F., Feely, R.A., Sabine, C.L., Atkinson, M.J., DeCarlo, E.H., MacKenzie, F.T., Drupp, P.S. and Butterfield, D.A. (2011) Calcification and organic production on a Hawaiian coral reef. Marine Chemistry 127, 6475.
Shapiro, S.S. and Wilk, M.B. (1965) An analysis of variance test for normality. Biometrika 52, 591599.
Song, C., Ballantyne, F. and Smith, V.H. (2013) Enhanced dissolved organic carbon production in aquatic ecosystems in response to elevated atmospheric CO2 . Biogeochemistry 118, 4960.
Strickland, J.D.H. (1960) Measuring the production of marine phytoplankton. Fisheries Research Board of Canada Bulletin 122, 172.
Strickland, J.D.H. and Parsons, T.R. (1968) A practical handbook of seawater analysis. Fisheries Research Board of Canada Bulletin 167, 293.
Sun, J. and Liu, D. (2003) Geometric models for calculating cell biovolume and surface area for phytoplankton. Journal of Plankton Research 25, 13311346.
Tang, D., Han, W., Li, P., Miao, X. and Zhong, J. (2011) CO2 biofixation and fatty acid composition of Scenedesmus obliquus and Chlorella pyrenoidosa in response to different CO2 levels. Bioresource Technology 102, 30713076.
Torres, R., Manriquez, P.H., Duarte, C., Navarro, J.M., Lagos, N.A., Vargas, C.A. and Lardies, M.A. (2013) Evaluation of a semi-automatic system for long-term seawater carbonate chemistry manipulation. Revista Chilena Historia Natural 86, 443451.
Tortell, P.D., Rau, G.H. and Morel, F.M.M. (2000) Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnology and Oceanography 45, 14851500.
Torstensson, A., Hedblom, M., Andersson, J., Andersson, M.X. and Wulff, A. (2013) Synergism between elevated pCO2 and temperature on the Antarctic sea ice diatom Nitzschia lecointei . Biogeosciences 10, 63916401.
Wingler, A., Quick, W.P., Bungard, R.A., Bailey, K.J., Lea, P.J. and Leegood, R.C. (1999) The role of photorespiration during drought stress: an analysis utilising barley mutants with reduced activities of photorespiratory enzymes. Plant Cell Environment 22, 361373.
Wohlers-Zöllner, J., Breithaupt, P., Walther, K., Jürgens, U. and Riebesell, U. (2011) Temperature and nutrient stoichiometry interactively modulate organic matter cycling in a pelagic algal-bacterial community. Limnology and Oceanography 56, 599610.
Wood, A.M. and Van Valen, L.M. (1990) Paradox lost? On the release of energy rich compounds by phytoplankton. Marine Microbial Food Webs 4, 103116.
Wu, Y., Gao, K. and Riebesell, U. (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum . Biogeosciences 7, 2.9152.923.
Wynn-Edwards, C., King, R., Davidson, A., Wright, S., Nichols, P.D., Simon, W., Kawagushi, S. and Vitue, P. (2014) Species-specific variations in the nutritional quality of southern ocean phytoplankton in response to elevated pCO2 . Water 6, 18401859.
Young, B.P., Shin, J.J.H., Orij, R., Chao, J.T., Li, S.C., Guan, X.L., Khong, A., Jan, E., Wenk, M.R., Prinz, W.A., Smits, G.J. and Loewen, C.J.R. (2010) Phosphatidic acid is a pH biosensor that links membrane biogenesis to metabolism. Science 329, 10851088.
Yu, P.C., Matson, P.G., Martz, T.R. and Hofmann, G.E. (2011) The ocean acidification seascape and its relationship to the performance of calcifiying marine invertebrates: laboratory experiments on the development of urchin larvae framed by environmentally-relevant pCO2/pH. Journal of Experimental Marine Biology and Ecology 400, 288295.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of the Marine Biological Association of the United Kingdom
  • ISSN: 0025-3154
  • EISSN: 1469-7769
  • URL: /core/journals/journal-of-the-marine-biological-association-of-the-united-kingdom
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed