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

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.

颗石藻（Coccolithophores）是一类可合成生物成因方解石鳞片的单细胞海洋藻类，对海洋初级生产及向深海的碳输出具有重要贡献。当前持续加剧的海洋酸化（ocean acidification）会显著损伤钙化生物，多数表现为生长与钙化作用的减弱。近期研究表明，赫氏颗石藻（Emiliania huxleyi）对海洋酸化的即时生理响应，可通过进化适应得到部分补偿，但其背后的潜在分子机制目前仍未明确。本研究测定了10个被推测与pH调控、碳转运、钙化作用及光合作用相关的候选基因的表达水平，实验对象分为两类：一类是经过驯化后短期暴露于海洋酸化环境的赫氏颗石藻种群（对应即时生理响应），另一类是经过500代高CO2驯化适应的赫氏颗石藻种群（对应适应性响应）。生理响应组的候选基因呈现下调表达，这与同期观测到的生长与钙化作用减弱的现象高度吻合。而在适应性响应组中，参与pH调控与碳转运的候选基因出现上调表达，这与高CO2驯化种群的生长与钙化作用部分恢复的结果一致。赫氏颗石藻对海洋酸化的适应可能依赖于细胞pH调控能力的提升，进而间接影响钙化作用。因此，适应性进化或可部分恢复细胞的pH调控能力，从而缓解海洋酸化带来的不良影响。