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，在海洋初级生产及碳向深海输出过程中发挥重要贡献。持续海洋酸化会对钙化生物造成显著损害，主要导致其生长与钙化作用减弱。已有研究显示，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。本研究针对两类赫氏颗石藻种群，分析了10个推定与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：一类为经过驯化后短期暴露于海洋酸化条件下的种群（对应即时生理响应），另一类为经过500代高CO₂驯化后的种群（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现象高度契合。而在适应性响应组中，推定的pH调控与碳转运基因出现上调表达，该结果与高CO₂驯化种群的生长与钙化作用部分恢复的现象相匹配。赫氏颗石藻对海洋酸化的适应性进化可能涉及细胞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利影响。