Seawater carbonate chemistry, tissue-skeleton interface and calcification in reef corals in a laboratory experiment

Insight into the response of reef corals and other major marine calcifiers to ocean acidification is limited by a lack of knowledge about how seawater pH and carbonate chemistry impact the physiological processes that drive biomineralization. Ocean acidification is proposed to reduce calcification rates in corals by causing declines in internal pH at the calcifying tissue-skeleton interface where biomineralization takes place. Here, we performed an in vivo study on how partial-pressure CO(2)-driven seawater acidification impacts intracellular pH in coral calcifying cells and extracellular pH in the fluid at the tissue-skeleton interface [subcalicoblastic medium (SCM)] in the coral Stylophora pistillata. We also measured calcification in corals grown under the same conditions of seawater acidification by measuring lateral growth of colonies and growth of aragonite crystals under the calcifying tissue. Our findings confirm that seawater acidification decreases pH of the SCM, but this decrease is gradual relative to the surrounding seawater, leading to an increasing pH gradient between the SCM and seawater. Reductions in calcification rate, both at the level of crystals and whole colonies, were only observed in our lowest pH treatment when pH was significantly depressed in the calcifying cells in addition to the SCM. Overall, our findings suggest that reef corals may mitigate the effects of seawater acidification by regulating pH in the SCM, but they also highlight the role of calcifying cell pH homeostasis in determining the response of reef corals to changes in external seawater pH and carbonate chemistry.学界对礁珊瑚（reef corals）及其他主要海洋钙化生物（marine calcifiers）如何响应海洋酸化（ocean acidification）的认知局限，源于尚未明确海水pH与碳酸盐化学（carbonate chemistry）如何调控驱动生物矿化（biomineralization）的生理过程。现有研究假说认为，海洋酸化会通过降低生物矿化发生处——钙化组织-骨骼界面的细胞内pH，抑制珊瑚的钙化速率。本研究以尖枝轴孔珊瑚（Stylophora pistillata）为实验材料，开展体内实验，探究二氧化碳分压（partial-pressure CO₂）驱动的海水酸化如何影响其钙化细胞的细胞内pH（intracellular pH），以及组织-骨骼界面处体液（即下皮层介质（subcalicoblastic medium, SCM））的细胞外pH。本研究同时通过测量珊瑚群落的侧向生长速率，以及钙化组织下方文石晶体（aragonite crystals）的生长情况，量化了相同海水酸化条件下珊瑚的钙化水平。研究结果证实，海水酸化会降低SCM的pH，但该降幅相较于周围海水更为平缓，导致SCM与海水之间的pH梯度逐渐增大。仅在最低pH处理组中，当钙化细胞与SCM的pH均显著降低时，我们才观测到晶体与珊瑚群落整体层面的钙化速率下降。综上，本研究结果表明，礁珊瑚可通过调控SCM的pH缓解海水酸化带来的负面影响，但同时也凸显了钙化细胞的pH稳态（pH homeostasis）在决定礁珊瑚响应外部海水pH与碳酸盐化学变化过程中的关键作用。