Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Variation in plastic responses of a globally distributed picoplankton species to ocean acidification

Nature Climate Change volume 3, pages 298–302 (2013)Cite this article

Subjects

Abstract

Phytoplankton are the basis of marine food webs, and affect biogeochemical cycles. As CO2 levels increase, shifts in the frequencies and physiology of ecotypes within phytoplankton groups will affect their nutritional value and biogeochemical function. However, studies so far are based on a few representative genotypes from key species. Here, we measure changes in cellular function and growth rate at atmospheric CO2 concentrations predicted for the year 2100 in 16 ecotypes of the marine picoplankton Ostreococcus. We find that variation in plastic responses among ecotypes is on par with published between-genera variation, so the responses of one or a few ecotypes cannot estimate changes to the physiology or composition of a species under CO2 enrichment. We show that ecotypes best at taking advantage of CO2 enrichment by changing their photosynthesis rates most should increase in relative fitness, and so in frequency in a high-CO2 environment. Finally, information on sampling location, and not phylogenetic relatedness, is a good predictor of ecotypes likely to increase in frequency in this system.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Physiological changes in O. tauri in response to elevated CO2 levels.
Figure 2: Variability of O. tauri ecotypes in photosynthesis and μ after acclimation to 1,000 ppm CO2.

References

  1. Vaulot, D., Eikrem, W., Viprey, M. & Moreau, H. The diversity of small eukaryotic phytoplankton <3 μm in marine ecosystems. FEMS Microbiol. Rev. 32, 795–820 (2008).

    Article  CAS  Google Scholar 

  2. Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. Ocean acidification: The other CO2 problem. Annu. Rev. Marine. Sci. 1, 169–192 (2009).

    Article  Google Scholar 

  3. Riebesell, U. et al. Enhanced biological carbon consumption in a high CO2 ocean. Nature 450, 545–548 (2007).

    Article  CAS  Google Scholar 

  4. Sterner, R., Hagemeier, D., Smith, W. & Smith, R. Phytoplankton nutrient limitation and food quality for Daphnia. Limnol. Oceanogr. 38, 857–871 (1993).

    Article  Google Scholar 

  5. Hoppe, C. J. M., Langer, G. & Rost, B. Emiliania huxleyi shows identical responses to elevated pCO2 in TA and DIC manipulations. J. Exp. Mar. Biol. Ecol. 406, 54–62 (2010).

    Article  Google Scholar 

  6. Kranz, S. A., Eichner, M. & Rost, B. Interactions between CCM and N2 fixation in Trichodesmium. Photosynth. Res. 109, 73–84 (2010).

    Article  Google Scholar 

  7. Rossoll, D. et al. Ocean acidification-induced food quality deterioration constrains trophic transfer. PLoS ONE 7, e34737 (2012).

    Article  CAS  Google Scholar 

  8. Langer, G., Nehrke, G., Probert, I., Ly, J. & Ziveri, P. Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6, 2637–2646 (2009).

    Article  CAS  Google Scholar 

  9. Fabry, V. J., Seibel, B. A., Feely, R. A. & Orr, J. C. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES. J. Mar. Sci. 65, 414–432 (2008).

    Article  CAS  Google Scholar 

  10. Le Quere, C. et al. Ecosystem dynamics based on plankton functional types for global ocean biogeochemistry models. Glob. Change Biol. 11, 2016–2040 (2005).

    Google Scholar 

  11. Courties, C. et al. Smallest eukaryotic organism. Nature 370, 255–255 (1994).

    Article  Google Scholar 

  12. Rodrı´guez, F. et al. Ecotype diversity in the marine picoeukaryoteOstreococcus (Chlorophyta, Prasinophyceae). Environ. Microbiol. 7, 853–859 (2005).

    Article  Google Scholar 

  13. Demir-Hilton, E. et al. Global distribution patterns of distinct clades of the photosynthetic picoeukaryote Ostreococcus. ISME J. 5, 1095–1107 (2011).

    Article  CAS  Google Scholar 

  14. Worden, A., Nolan, J. & Palenik, B. Assessing the dynamics and ecology of marine picophytoplankton: The importance of the eukaryotic component. Limnol. Oceanogr. 49, 168–179 (2004).

    Article  CAS  Google Scholar 

  15. Elser, J., Hayakawa, K. & Urabe, J. Nutrient limitation reduces food quality for zooplankton: Daphnia response to seston phosphorus enrichment. Ecology 82, 898–903 (2001).

    Article  Google Scholar 

  16. Egleston, E. S., Sabine, C. L. & Morel, F. M. M. Revelle revisited: Buffer factors that quantify the response of ocean chemistry to changes in DIC and alkalinity. Glob. Biogeochem. Cycles 24, GB1002 (2010).

    Article  Google Scholar 

  17. Collins, S. & Bell, G. Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature 431, 566–569 (2004).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  19. Fu, F. X. et al. Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera. Limnol. Oceanogr. 6, 2472–2484 (2008).

    Article  Google Scholar 

  20. Sterner, R. & Elser, J. Ecological Stoichiometry: The Biology of Elements from co2 Molecules to the Biosphere (Princeton Univ. Press, 2002).

    Google Scholar 

  21. Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Natural. 138, 1315–1341 (1991).

    Article  Google Scholar 

  22. Collins, S. Many possible worlds: Expanding the ecological scenarios in experimental evolution. Evol. Biol. 38, 3–14 (2011).

    Article  Google Scholar 

  23. Tortell, P. D. et al. CO2 sensitivity of Southern Ocean phytoplankton. Geophys. Res. Lett. 35, L04605 (2008).

    Article  Google Scholar 

  24. Copin-Montégut, C., Bégovic, M. & Merlivat, L. Variability of the partial pressure of CO2 on diel to annual time scales in the Northwestern Mediterranean Sea. Mar. Chem. 85, 169–189 (2004).

    Article  Google Scholar 

  25. Takahashi, T. et al. Corrigendum to ‘Climatological mean and decadal change in surface ocean pCO2, and net sea–air CO2 flux over the global oceans’ (Deep Sea Res. II 56, 554–577 (2009)). Deep-Sea Res. I 56, 2075–2076 (2009).

    Article  Google Scholar 

  26. Mueller, M. N., Schulz, K. G. & Riebesell, U. Effects of long-term high CO2 exposure on two species of coccolithophores. Biogeosciences 7, 1109–1116 (2010).

    Article  Google Scholar 

  27. Van de Waal, D. B. et al. Reversal in competitive dominance of a toxic versus non-toxic cyanobacterium in response to rising CO2 . ISME J. 5, 1438–1450 (2011).

    Article  CAS  Google Scholar 

  28. Keller, M. D., Selvin, R. C., Claus, W. & Guillard, R. Media for the culture of oceanic ultra phytoplankton. J. Phycol. 23, 633–638 (1987).

    Article  Google Scholar 

  29. Lewis, E. & Wallace, D. Program Developed for the CO 2 System Calculations (Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, 1998).

  30. Rokitta, S. & Rost, B. Effects of CO2 and their modulation by light in the life-cycle stages of the coccolithophore Emiliania huxleyi. Limnol. Oceanogr. 57, 607–618 (2012).

    Article  CAS  Google Scholar 

  31. Levitan, O. et al. Elevated CO2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob. Change Biol. 13, 531–538 (2007).

    Article  Google Scholar 

  32. Barcelos e Ramos, J., Biswas, H., Schulz, K. G., LaRoche, J. & Riebesell, U. Effect of rising atmospheric carbon dioxide on the marine nitrogen fixer Trichodesmium. Glob. Biogeochem. Cycles 21, GB2028 (2007).

    Article  Google Scholar 

  33. Hutchins, D., Fu, F., Zhang, Y. & Warner, M. CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr. 52, 1293–1304 (2007).

    Article  CAS  Google Scholar 

  34. Kranz, S., Sultemeyer, D., Richter, K. U. & Rost, B. Carbon acquisition in Trichodesmium: The effect of pCO2 and diurnal changes. Limnol. Oceanogr. 54, 548–559 (2009).

    Article  CAS  Google Scholar 

  35. Trimborn, S. et al. Inorganic carbon acquisition in potentially toxic and non-toxic diatoms: The effect of pH-induced changes in seawater carbonate chemistry. Phys. Plant 133, 92–105 (2008).

    Article  CAS  Google Scholar 

  36. Wu, Y., Gao, K. & Riebesell, U. CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7, 2915–2923 (2010).

    Article  CAS  Google Scholar 

  37. Hu, H. & Gao, K. Impacts of CO2 enrichment on growth and photosynthesis in freshwater and marine diatoms. Chin. J. Oceanol. Limnol. 26, 407–414 (2009).

    Article  Google Scholar 

  38. Langer, G. et al. Species-specific responses of calcifying algae to changing seawater carbonate chemistry. Geochem. Geophys. Geosyst. 7, Q09006 (2006).

    Article  Google Scholar 

  39. Lohbeck, K. T., Riebesell, U. & Reusch, T. B. H. Adaptive evolution of a key phytoplankton species to ocean acidification. Nature Geosci. 5, 346–351 (2012).

    Article  CAS  Google Scholar 

  40. Feng, Y. et al. Interactive effects of increased pCO2, temperature and irradiance on the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae). Eur. J. Phycol. 43, 87–98 (2008).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was conducted at the University of Edinburgh (UK) and the Alfred Wegener Institute for Polar and Marine Research (Germany). The research was supported by a Royal Society (UK) University Research Fellowship (S.C.), the European Research Council (ERC) under the European Community’s Seventh Framework Programme (FP7/2007-2013), ERC grant agreement 205150 (B.R.) and a Scottish Universities Life Science Alliance scholarship (E.S.). We thank M. Allen and ASSEMBLE (Association of European Marine Biology Laboratories) Roscoff for providing the Ostreococcus ecotypes; H. Kuehne, S. Reece and T. Reusch for advice on the manuscript; J. Raven for advice concerning the experiments; and S. Rokitta, K-U. and U. Richter for assistance in the laboratory at the AWI.

Author information

Authors and Affiliations

  1. University of Edinburgh, Institute of Evolutionary Biology, Ashworth Laboratories, West Mains Road, Edinburgh EH9 3JF, UK

    Elisa Schaum & Sinéad Collins

  2. Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen, 27570 Bremerhaven, Germany

    Björn Rost

  3. University of Edinburgh, Centre for Systems Biology at Edinburgh, C.H. Waddington Building, Mayfield Road, Edinburgh EH9 3JD, UK

    Andrew J. Millar

Authors
  1. Elisa Schaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Björn Rost
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrew J. Millar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sinéad Collins
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.S. designed and performed the experiments, analysed data and wrote the manuscript. S.C. designed the experiments, analysed data, wrote the manuscript and supervised laboratory work. B.R. supervised the laboratory work at the Alfred-Wegener-Institute and contributed to the manuscript. A.J.M. contributed to the manuscript.

Corresponding author

Correspondence to Elisa Schaum.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 1242 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Schaum, E., Rost, B., Millar, A. et al. Variation in plastic responses of a globally distributed picoplankton species to ocean acidification. Nature Clim Change 3, 298–302 (2013). https://doi.org/10.1038/nclimate1774

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate1774

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing