Long-term adaptation of the coccolithophore Emiliania huxleyi to ocean acidification and global warming

Humans are profoundly altering the carbon cycle by fossil fuel burning, which contributes directly and indirectly to global change. Excess anthropogenic CO2 emissions not only drive the greenhouse effects and atmospheric warming but also cause ocean acidification when CO2 dissolves in ocean waters. How marine phytoplankton reacts to these changes is of particular interest as it contributes almost half of the global carbon fixation. Especially calcifying marine organisms are sensitive to ocean acidification. This puts coccolithophores as calcite producing phytoplankton in the focus of research on global change impacts. Because of their short reproduction time and high population densities coccolithophores are the ideal candidate to investigate adaptive evolution to global change.

My study species, the coccolithophore Emiliania huxleyi is one of the most abundant phytoplankton in the ocean, and at the same time, can be cultured easily in the laboratory. Coccolithophore growth and calcification display temperature dependent CO2-optimum curves, which indicate a reduction in growth rate and calcification under future ocean conditions of warming and ocean acidification. While the potential of E. huxleyi to adapt to ocean acidification has already been shown, how warming and acidification adaptation interact remained uncertain. In my first chapter, I tested for the long-term effects of CO2 adaptation (1100 μatm pCO2, 2200 μatm pCO2) and the interactions with temperature adaptation (26.3°C) introduced after 1600 generations of CO2 adaptation.

Building upon first experiments over one year duration, I next assessed whether adaptation to ocean acidification alone would continue over a time interval of 4 yrs. The elongation of the selection to CO2 revealed that the long-term adaptation is complex and phenotypic responses may revert over time. After 2100 asexual generations of selection to CO2 the fitness (growth rate) increased slightly over time under medium CO2 conditions (1100 μatm pCO2). Under high CO2 (2200 μatm pCO2) the fitness advantage of 5% at 500 generations remained unchanged. The phenotypic trait of calcification was partly restored within 500 generations. Thereafter, calcification was reduced in response to selection. The reduction of calcification was not constitutively, as the calcite per cell quotas were restored when assessed with present-day CO2 conditions (400 μatm pCO2). Some phenotypic traits were likely associated with selection for higher growth rate, such as a reduced cell size and lower particulate organic carbon (POC) content per cell.

Temperature adaptation occurred independently of ocean acidification levels. The fitness increase in growth rate due was up to 16% in populations adapted to high temperature and high CO2 compared to not adapted cells under selection conditions. The ratio of particular inorganic (PIC) and organic carbon (PIC:POC) recovered to their initial ratio after temperature adaptation, even under elevated CO2. Cells evolved to a smaller size accompanied by a reduction in POC-content. Production rates were restored to values under present-day ocean conditions, owing to adaptive evolution in growth rate. They were 101% (PIC) and 55% (POC) higher under warming compared to the non-adapted controls.

In my third chapter, I addressed how temperature selection changed adaptation to ocean acidification. Temperature adaptation increased the effect on persisting CO2 adaptation in growth rate. The adaptive reduction of cell size to CO2 selection was reversed after temperature adaptation, leading to larger CO2 adapted cells at high temperature. The immediate physiological effect on PIC per cell was diminished compared to the lower temperature treatment, and so were the adaptive effects. Temperature adaptation reduced the negative effects of ocean acidification. Both adaptations were necessary to receive the full fitness effect under high-temperature-high-CO2-conditions. As consequence both adaptive effects are additive, with a slight and not significant tendency to synergistic, as the combined effect is slightly larger than the addition of both single effects.

Taken together, global warming may reduce the adverse effects of ocean acidification on E. huxleyi populations. My results show further, that marine phytoplankton may evolve changes in the plastic response under future ocean conditions. This could affect biogeochemical important traits, such as calcification, in an unpredictable way. Nevertheless, marine microbes like unicellular phytoplankton have quite good chances to adapt to ocean acidification and global warming, in contrast to many organisms with longer generation times.

Schlüter L., 2016. Long-term adaptation of the coccolithophore Emiliania huxleyi to ocean acidification and global warming. PhD thesis, Christian-Albrechts-Universität zu Kiel, 229 p. Thesis.

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