Hostname: page-component-7bb8b95d7b-w7rtg Total loading time: 0 Render date: 2024-10-03T11:21:57.780Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  21 November 2016

Bárbara G. Jacob*
Affiliation:
Department of Aquatic System, Aquatic Ecosystem Functioning Lab (LAFE), Faculty of Environmental Sciences & Environmental Sciences Center EULA Chile, Universidad de Concepción, Concepción 4070386, Chile
Peter von Dassow
Affiliation:
Instituto Milenio de Oceanografía (IMO), Universidad de Concepción, Concepción 4070386, Chile Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Avenida Bernardo O′Higgins 340, Santiago 8331150, Chile UMI 3614, Evolutionary Biology and Ecology of Algae, CNRS-UPMC Sorbonne Universités, PUCCh, UACH, Station Biologique de Roscoff, Roscoff 29682, France
Joe E. Salisbury
Affiliation:
Ocean Process Analysis Laboratory, University of New Hampshire, Durham, NH 03824, USA
Jorge M. Navarro
Affiliation:
Laboratorio Costero de Recursos Acuáticos de Calfuco, Facultad de Ciencias, Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Independencia 641, Valdivia 5110566, Chile Centro FONDAP de Investigación en Dinámica de Ecosistemas Marinos de Altas Latitudes (IDEAL), Universidad Austral de Chile, Valdivia, Chile
Cristian A. Vargas
Affiliation:
Department of Aquatic System, Aquatic Ecosystem Functioning Lab (LAFE), Faculty of Environmental Sciences & Environmental Sciences Center EULA Chile, Universidad de Concepción, Concepción 4070386, Chile Instituto Milenio de Oceanografía (IMO), Universidad de Concepción, Concepción 4070386, Chile Center for the Study of Multiple-Drivers on Marine Socio-Ecological Systems (MUSELS), Universidad de Concepción, Concepción, Chile
*
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: bjacob@udec.cl

Abstract

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.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alldredge, A.L. and Jackson, G.A. (1995) Aggregation in marine systems. Deep-Sea Research II 42, 17.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Borchard, C. and Engel, A. (2012) Organic matter exudation by Emiliania huxleyi under simulated future ocean conditions. Biogeosciences 9, 34053423.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Caldeira, K. and Wickett, M.E. (2003) Anthropogenic carbon and ocean pH. Nature 425, 365.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Di Martino, C., Delne, S., Alvino, A. and Loreto, F. (1999) Photorespiration rate in spinach leaves under moderate NaCl stress. Photosynthetica 36, 233242.CrossRefGoogle Scholar
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 http://cdiac.ornl.gov/oceans/DOE_94.pdf Google Scholar
Downton, W.J.S. (1977) Photosynthesis in salt-stressed grapevines. Australian Journal of Plant Physiology 4, 183192.Google Scholar
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.CrossRefGoogle Scholar
Engel, A. (2002) Direct relationship between CO2 uptake and transparent exopolymer particles production in natural phytoplankton. Journal of Plankton Research 24, 4953.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Hessen, D.O., Ågren, G.I. and Anderson, T.R. (2004) Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85, 11791192.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Hofmann, D., Butler, J.H. and Tans, P.P. (2011) A new look at atmospheric carbon dioxide. Atmospheric Environment 43, 20842086.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle Scholar
Lorenzen, C.J. (1966) A method for the continuous measurement of in vivo chlorophyll concentration. Deep Sea Research 13, 223227.Google Scholar
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.CrossRefGoogle Scholar
Mackey, R.M., Morris, J.J., Morel, F.M.M. and Kranz, S.A. (2015) Response of photosynthesis to ocean acidification. Oceanography 28, 7491.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Passow, U. (2002) Transparent exopolymer particles (TEP) in aquatic environment. Progress in Oceanography 55, 287333.CrossRefGoogle Scholar
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 http://cdiac.ornl.gov/ftp/co2sys Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Rost, B., Riebesell, U., Burkhardt, S. and Sültemeyer, D. (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnology and Oceanography 48, 5567.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Shapiro, S.S. and Wilk, M.B. (1965) An analysis of variance test for normality. Biometrika 52, 591599.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Strickland, J.D.H. (1960) Measuring the production of marine phytoplankton. Fisheries Research Board of Canada Bulletin 122, 172.Google Scholar
Strickland, J.D.H. and Parsons, T.R. (1968) A practical handbook of seawater analysis. Fisheries Research Board of Canada Bulletin 167, 293.Google Scholar
Sun, J. and Liu, D. (2003) Geometric models for calculating cell biovolume and surface area for phytoplankton. Journal of Plankton Research 25, 13311346.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar