Genes Related to Ion-Transport and Energy Production Are Upregulated in Response to CO2-Driven pH Decrease in Corals: New Insights from Transcriptome Analysis

Since the preindustrial era, the average surface ocean pH has declined by 0.1 pH units and is predicted to decline by an additional 0.3 units by the year 2100. Although subtle, this decreasing pH has profound effects on the seawater saturation state of carbonate minerals and is thus predicted to impact on calcifying organisms. Among these are the scleractinian corals, which are the main builders of tropical coral reefs. Several recent studies have evaluated the physiological impact of low pH, particularly in relation to coral growth and calcification. However, very few studies have focused on the impact of low pH at the global molecular level. In this context we investigated global transcriptomic modifications in a scleractinian coral (Pocillopora damicornis) exposed to pH 7.4 compared to pH 8.1during a 3-week period. The RNAseq approach shows that 16% of our transcriptome was affected by the treatment with 6% of upregulations and 10% of downregulations. A more detailed analysis suggests that the downregulations are less coordinated than the upregulations and allowed the identification of several biological functions of interest. In order to better understand the links between these functions and the pH, transcript abundance of 48 candidate genes was quantified by q-RT-PCR (corals exposed at pH 7.2 and 7.8 for 3 weeks). The combined results of these two approaches suggest that pH≥7.4 induces an upregulation of genes coding for proteins involved in calcium and carbonate transport, conversion of CO2 into HCO3− and organic matrix that may sustain calcification. Concomitantly, genes coding for heterotrophic and autotrophic related proteins are upregulated. This can reflect that low pH may increase the coral energy requirements, leading to an increase of energetic metabolism with the mobilization of energy reserves. In addition, the uncoordinated downregulations measured can reflect a general trade-off mechanism that may enable energy reallocation.自前工业化时代以来，海洋表层平均pH已下降0.1个pH单位，且预测到2100年还将再下降0.3个单位。尽管这一变化看似微小，但会显著改变碳酸盐矿物在海水中的饱和状态，因此预计会对钙化生物产生影响。其中造礁石珊瑚（scleractinian corals）是热带珊瑚礁的主要建造者。近年来已有多项研究评估了低pH的生理学影响，尤其是围绕珊瑚生长与钙化过程的相关效应。然而，极少有研究聚焦于全球分子层面的低pH影响。在此研究背景下，我们对暴露于pH7.4与pH8.1环境、为期3周的造礁石珊瑚（Pocillopora damicornis）开展了全球转录组表达变化分析。转录组测序（RNAseq）结果显示，本研究的转录组中有16%受到实验处理的影响，其中6%呈上调表达，10%呈下调表达。进一步的详细分析表明，下调基因的调控协调性弱于上调基因，并由此鉴定出多个值得关注的生物学功能。为进一步明晰这些功能与pH之间的关联，我们通过定量实时聚合酶链反应（q-RT-PCR）对48个候选基因的转录本丰度进行了定量分析，实验对象为暴露于pH7.2、pH7.8环境下为期3周的珊瑚。两种实验方法的联合分析结果表明，当pH≥7.4时，参与钙与碳酸盐转运、CO₂转化为HCO₃⁻以及维持钙化过程的有机基质相关蛋白的编码基因均呈现上调表达。与此同时，与异养和自养相关的蛋白编码基因也出现上调。这一现象可反映出低pH环境可能提升珊瑚的能量需求，进而通过动员能量储备增强能量代谢。此外，本研究观测到的协调性较弱的下调基因表达模式，可能反映了一种通用的能量分配权衡机制。