Gene expression changes in the coccolithophore Emiliania huxleyi after 500 generations of selection to ocean acidification

Abstract

Coccolithophores are unicellular marine algae that produce biogenic calcite scales and substantially contribute to marine primary production and carbon export to the deep ocean. Ongoing ocean acidification particularly impairs calcifying organisms, mostly resulting in decreased growth and calcification. Recent studies revealed that the immediate physiological response in the coccolithophore Emiliania huxleyi to ocean acidification may be partially compensated by evolutionary adaptation, yet the underlying molecular mechanisms are currently unknown. Here, we report on the expression levels of 10 candidate genes putatively relevant to pH regulation, carbon transport, calcification and photosynthesis in E. huxleyi populations short-term exposed to ocean acidification conditions after acclimation (physiological response) and after 500 generations of high CO2 adaptation (adaptive response). The physiological response revealed downregulation of candidate genes, well reflecting the concomitant decrease of growth and calcification. In the adaptive response, putative pH regulation and carbon transport genes were up-regulated, matching partial restoration of growth and calcification in high CO2-adapted populations. Adaptation to ocean acidification in E. huxleyi likely involved improved cellular pH regulation, presumably indirectly affecting calcification. Adaptive evolution may thus have the potential to partially restore cellular pH regulatory capacity and thereby mitigate adverse effects of ocean acidification.

Keywords: adaptation; calcification; gene expression; ocean acidification; phytoplankton.

Figure 1.

Physiological response in relative gene expression of 10 candidate genes in replicated (N = 5) ambient pCO₂ (400 µatm)-adapted control populations when tested under medium (1100 µatm) and high (2200 µatm) pCO₂ conditions. Differences in mean gene expression levels are illustrated as fold expression change ± s.e.m. Pale bars indicate relative gene expression of control populations assayed at 1100 µatm pCO₂ relative to control populations assayed at 400 µatm pCO₂. Dark bars indicate gene expression of control populations assayed at 2200 µatm pCO₂ relative to control populations assayed at 400 µatm pCO₂. Significance levels are indicated: *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001.

Figure 2.

Adaptive response in relative gene expression of 10 candidate genes in replicated (N = 5) medium and high CO₂-adapted E. huxleyi populations. Differences in mean gene expression levels between CO₂-adapted and control populations are illustrated as fold expression change ± s.e.m. Pale bars indicate gene expression in populations adapted to 1100 µatm pCO₂ relative to control populations adapted to 400 µatm pCO₂ when tested under 1100 µatm pCO₂. Dark bars indicate gene expression in populations adapted to 2200 µatm pCO₂ relative to control populations adapted to 400 µatm pCO₂ when tested under 2200 µatm pCO₂. Significance levels are indicated: *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001.