Marine phytoplankton can adapt to ocean acidification

Kai Lohbeck is a PhD student in the BIOACID project at GEOMAR (Kiel, Germany). His interdisciplinary work combines biological oceanography and evolutionary biology to investigate the potential for evolutionary adaptation to ocean acidification in marine phytoplankton.

The uptake of fossil fuel-derived carbon dioxide by the surface ocean alters seawater carbonate chemistry and results in a drop in ocean pH (Caldeira and Wickett 2003). These changes, dubbed ocean acidification, have a severe impact on many marine organisms, especially those that build their cell walls, shells, scales or skeletons from calcium carbonate (Orr et al., 2005).

Coccolithophores, a group of planktonic microalgae that are among the most productive calcifying organisms in the sea (Westbroek et al., 1989), were found to be sensitive to ocean acidification with most studies showing a decline in growth and calcification rate at increased CO2 levels (Riebesell and Tortell 2011).

Such studies have usually been short term (a couple of weeks) and none tested for evolutionary adaptation, a major unknown when attempting to predict future impacts of ocean acidification on marine life (Riebesell et al., 2009). As coccolithophore populations reproduce quickly and have large population sizes, they should be particularly prone to respond to ocean change via adaptive evolution (Bell and Collins 2008).

To test whether marine phytoplankton can adapt to ocean acidification, we conducted two long-term laboratory selection experiments where we exposed replicate populations of the coccolithophore Emiliania huxleyi for about one year to elevated CO2 levels. One experiment started from replicated populations assembled from equal contributions of six different clones and the other from replicates originating from a single clone. The multi-clone experiment was designed to provide standing genetic variation that would allow population-level adaptation by genotypic selection, whereas in the single- clone experiment adaptation requires new mutations (Lohbeck et al., 2012).

Replicate selection lines were grown for about 500 asexual generations at ambient (400 μatm), medium (1100 μatm) and high (2200 μatm) levels of CO2 partial pressure. The medium-CO2 treatment represented a level projected for the beginning of the next century while the highest level served as a proof of principle, representing a sufficiently strong selective force. To test for adaptation we then compared populations grown under increased CO2 levels with those kept under ambient CO2 levels in an increased CO2 assay environment (Lohbeck et al., 2012).

Our study identified direct, positive adaptation to increased CO2 levels in a calcifying marine phytoplankton species. In both experiments, E. huxleyi populations adapted to elevated CO2 conditions and showed significantly increased exponential growth rates (a direct measure of Darwinian fitness) and partly restored calcification rates relative to control populations when tested under ocean acidification conditions (Fig. 1). In the multi-clone experiment the presence of the six experimental clones throughout the experiment was examined using microsatellite genotyping. The genotypic composition of the populations diverged consistently among treatments (Fig. 2).

We identified genotypic selection as one immediate mechanism of population-level adaptation in the multi-clone experiment. The adaptive response observed in the single- clone experiment suggests a contribution of advantageous new mutations.

Coccolithophores play an important role in ocean productivity and the marine carbon cycle (Westbroek et al., 1989). Hence, the swift adaptation processes observed here have the potential to affect food-web dynamics and biogeochemical cycles on climate change-relevant timescales. Our findings emphasize the need to consider evolutionary processes in future studies on the biological consequences of global change.

As experimental evolution experiments reveal only the potential for adaptation, they need to be further scrutinized against field observations to assess to what extent evolutionary changes observed under laboratory conditions apply in the oceans, where other environmental factors and ecological interactions play along.

References

Bell, G., and S. Collins. (2008). Adaptation, extinction and global change. Evol. Appl. 1:3-16.
Caldeira, K., and M. E. Wickett. (2003). Anthropogenic carbon and ocean pH. Nature 425:365-365.
Lohbeck, K. T., et al. (2012). Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 5:346-351.
Orr, J. C., et al. (2005). Anthropogenic ocean acidification over the twenty- first century and its impact on calcifying organisms. Nature 437:681-686.
Riebesell, U., et al. (2009). Sensitivities of marine carbon fluxes to ocean change. Proc. Natl. Acad. Sci. U. S. A. 106:20602-20609.
Riebesell, U., and P. D. Tortell. (2011). Effects of ocean acidification on pelagic organisms and ecosystems. Pp. 99-121 in J.-P. Gattuso, Hansson, L., ed. Ocean Acidification. Oxford Univ. Press, Oxford, U.K.
Westbroek, P., et al. (1989). Coccolith Production (Biomineralization) in the Marine Alga Emiliania huxleyi. J. Protozool. 36:368-373.

Acknowledgements

This work was funded by the German Federal Ministry of Education and Research (BMBF).

Lohbeck K., Riebesell U. & Reusch T., 2013. Marine phytoplankton can adapt to ocean acidification. SOLAS NEWS 15, Summer 2013: 26-27. Article.

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