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Adaptive evolution of a key phytoplankton species to ocean acidification

Nature Geoscience volume 5, pages 346–351 (2012)Cite this article

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A Corrigendum to this article was published on 29 November 2012

This article has been updated

Abstract

Ocean acidification, the drop in seawater pH associated with the ongoing enrichment of marine waters with carbon dioxide from fossil fuel burning, may seriously impair marine calcifying organisms. Our present understanding of the sensitivity of marine life to ocean acidification is based primarily on short-term experiments, in which organisms are exposed to increased concentrations of CO2. However, phytoplankton species with short generation times, in particular, may be able to respond to environmental alterations through adaptive evolution. Here, we examine the ability of the world’s single most important calcifying organism, the coccolithophore Emiliania huxleyi, to evolve in response to ocean acidification in two 500-generation selection experiments. Specifically, we exposed E. huxleyi populations founded by single or multiple clones to increased concentrations of CO2. Around 500 asexual generations later we assessed their fitness. Compared with populations kept at ambient CO2 partial pressure, those selected at increased partial pressure exhibited higher growth rates, in both the single- and multiclone experiment, when tested under ocean acidification conditions. Calcification was partly restored: rates were lower under increased CO2 conditions in all cultures, but were up to 50% higher in adapted compared with non-adapted cultures. We suggest that contemporary evolution could help to maintain the functionality of microbial processes at the base of marine food webs in the face of global change.

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Figure 1: Phenotypic responses to ∼ 500 generations of selection in E. huxleyi.
Figure 2: Time course of the presence of E. huxleyi genotypes in the multiclone experiment.
Figure 3: Response of correlated traits after selection to increased CO2 levels in the coccolithophore E. huxleyi.

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  • 20 November 2012

    In the version of this article originally published, the y axis scales of Fig. 3c–f were incorrect. This has been corrected in the PDF and HTML versions.

References

  1. Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).

    Article  Google Scholar 

  2. Feely, R. A. et al. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305, 362–366 (2004).

    Article  Google Scholar 

  3. Caldeira, K. & Wickett, M. E. Oceanography: Anthropogenic carbon and ocean pH. Nature 425, 365–365 (2003).

    Article  Google Scholar 

  4. 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  Google Scholar 

  5. Frommel, A. Y. et al. Severe tissue damage in Atlantic cod larvae under increasing ocean acidification. Nature Clim. Change 2, 42–46 (2012).

    Article  Google Scholar 

  6. Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).

    Article  Google Scholar 

  7. Fabricius, K. E. et al. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Clim. Change 1, 165–169 (2011).

    Article  Google Scholar 

  8. Hall-Spencer, J. M. et al. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454, 96–99 (2008).

    Article  Google Scholar 

  9. Westbroek, P., Young, J. R. & Linschooten, K. Coccolith production (biomineralization) in the marine alga Emiliania huxleyi. J. Eukaryot. Microbiol. 36, 368–373 (1989).

    Google Scholar 

  10. Armstrong, R. A., Lee, C., Hedges, J. I., Honjo, S. & Wakeham, S. G. A new, mechanistic model for organic carbon fluxes in the ocean based on the quantitative association of POC with ballast minerals. Deep-Sea Res. II 49, 219–236 (2001).

    Article  Google Scholar 

  11. Riebesell, U. et al. Reduced calcification of marine plankton in response to increased atmospheric CO2 . Nature 407, 364–367 (2000).

    Article  Google Scholar 

  12. Zondervan, I. The effects of light, macronutrients, trace metals and CO2 on the production of calcium carbonate and organic carbon in coccolithophores—a review. Deep-Sea Res. II 54, 521–537 (2007).

    Article  Google Scholar 

  13. Riebesell, U. & Tortell, P. D. in Ocean Acidification (eds Gattuso, J-P. & Hansson, L.) 99–121 (Oxford Univ. Press, 2011).

    Google Scholar 

  14. Collins, S. Comment on Effects of long-term high CO2 exposure on two species of coccolithophores by Müller et al. (2010). Biogeosci. Disc. 7, 2673–2679 (2010).

    Article  Google Scholar 

  15. Riebesell, U., Körtzinger, A. & Oschlies, A. Sensitivities of marine carbon fluxes to ocean change. Proc. Natl Acad. Sci. USA 106, 20602–20609 (2009).

    Article  Google Scholar 

  16. Joint, I., Doney, S. C. & Karl, D. M. Will ocean acidification affect marine microbes? ISME J. 5, 1–7 (2011).

    Article  Google Scholar 

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

    Article  Google Scholar 

  18. Hoffmann, A. A. & Sgro, C. M. Climate change and evolutionary adaptation. Nature 470, 479–485 (2011).

    Article  Google Scholar 

  19. Reusch, T. B. H. & Wood, T. E. Molecular ecology of global change. Mol. Ecol. 16, 3973–3992 (2007).

    Article  Google Scholar 

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

    Article  Google Scholar 

  21. Elena, S. F. & Lenski, R. E. Evolution experiments with microorganisms: The dynamics and genetic bases of adaptation. Nature Rev. Genet. 4, 457–469 (2003).

    Article  Google Scholar 

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

    Article  Google Scholar 

  23. Becks, L., Ellner, S. P., Jones, L. E. & Hairston, N. G. Jr Reduction of adaptive genetic diversity radically alters eco-evolutionary community dynamics. Ecol. Lett. 13, 989–997 (2010).

    Google Scholar 

  24. IPCC Climate Change 2007: Impacts, Adaptation and Vulnerability (eds Parry, M. L., Canziani, O. F., Palutikof, J. P., van der Linden, P. J. & Hanson, C. E.) (Cambridge Univ. Press, 2007).

  25. Feely, R. A., Sabine, C. L., Hernandez-Ayon, J. M., Ianson, D. & Hales, B. Evidence for upwelling of corrosive ‘acidified’ water onto the continental shelf. Science 320, 1490–1492 (2008).

    Article  Google Scholar 

  26. Bennett, A. F. & Lenski, R. E. Evolutionary adaptation to temperature. II thermal niches of experimental lines of Escherichia coli. Evolution 47, 1–12 (1993).

    Article  Google Scholar 

  27. Lenski, R. E. et al. Evolution of competitive fitness in experimental populations of E. coli: What makes one genotype a better competitor than another? Anton. van Leeuw. 73, 35–47 (1998).

    Article  Google Scholar 

  28. Gerrish, P. & Lenski, R. The fate of competing beneficial mutations in an asexual population. Genetica 102–103, 127–144 (1998).

    Article  Google Scholar 

  29. Zondervan, I., Zeebe, R. E., Rost, B. & Riebesell, U. A time series study of silica production and flux in an eastern boundary region: Santa Barbara Basin, California. Glob. Biogeochem. Cycles 15, 507–516 (2001).

    Article  Google Scholar 

  30. Mackinder, L. et al. Expression of biomineralization-related ion transport genes in Emiliania huxleyi. Environ. Microbiol. 13, 3250–3265 (2011).

    Article  Google Scholar 

  31. Paasche, E. A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions. Phycologia 40, 503–529 (2002).

    Article  Google Scholar 

  32. Zeyl, C., Vanderford, T. & Carter, M. An evolutionary advantage of haploidy in large yeast populations. Science 299, 555–558 (2003).

    Article  Google Scholar 

  33. Desai, M. M., Fisher, D. S. & Murray, A. W. The speed of evolution and maintenance of variation in asexual populations. Curr. Biol. 17, 385–394 (2007).

    Article  Google Scholar 

  34. Travisano, M., Vasi, F. & Lenski, R. E. Long-term experimental evolution in Escherichia coli. III. Variation among replicate populations in correlated responses to novel environments. Evolution 49, 189–200 (1995).

    Google Scholar 

  35. Iglesias-Rodriguez, M. D., Schofield, O. M., Batley, J., Medlin, L. K. & Hayes, P. K. Intraspecific genetic diversity in the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae): The use of microsatellite analysis in marine phytoplankton population studies. J. Phycol. 42, 526–536 (2006).

    Article  Google Scholar 

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

    Article  Google Scholar 

  37. Kaltz, O. & Bell, G. The ecology and genetics of fitness in Chlamydomonas. XII: Repeated sexual episodes increase rates of adaptation to novel environments. Evolution 56, 1743–1753 (2002).

    Article  Google Scholar 

  38. Beaufort, L. et al. Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476, 80–83 (2011).

    Article  Google Scholar 

  39. Falkowski, P. G. & Oliver, M. J. Mix and match: How climate selects phytoplankton. Nature Rev. Microbiol. 5, 813–819 (2007).

    Article  Google Scholar 

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Acknowledgements

We thank J. Meyer, A. Zavišić, K. Beining, A. Ludwig, S. Fessler and P. Fritsche for laboratory assistance; J. Czerny and C. Eizaguirre for advice on the experimental design, H. Schulenburg, J. Olsen and O. Roth for comments on earlier drafts; L. Bach, S. Febiri, T. Großkopf, L. Mackinder, D. Haase and K. Schulz for support during the experiments. T.B.H.R. and U.R. received financial support for this project from the German Federal Ministry of Education and Research (BMBF; project BIOACID).

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Authors and Affiliations

  1. Evolutionary Ecology of Marine Fishes, Helmholtz-Centre for Ocean Research Kiel (GEOMAR), Düsternbrooker Weg 20, 24105 Kiel, Germany

    Kai T. Lohbeck & Thorsten B. H. Reusch

  2. Biological Oceanography, Helmholtz-Centre for Ocean Research Kiel (GEOMAR), Düsternbrooker Weg 20, 24105 Kiel, Germany

    Kai T. Lohbeck & Ulf Riebesell

Authors
  1. Kai T. Lohbeck
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  3. Thorsten B. H. Reusch
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Contributions

T.B.H.R. conceived the project, all authors designed the experiment and K.T.L. carried out the experiment. All authors analysed and interpreted the data and wrote the manuscript.

Corresponding author

Correspondence to Thorsten B. H. Reusch.

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The authors declare no competing financial interests.

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Lohbeck, K., Riebesell, U. & Reusch, T. Adaptive evolution of a key phytoplankton species to ocean acidification. Nature Geosci 5, 346–351 (2012). https://doi.org/10.1038/ngeo1441

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