Sodium provides unique insights into transgenerational effects of ocean acidification on bivalve shell formation

Ocean acidification is likely to have profound impacts on marine bivalves, especially on their early life stages. Therefore, it is imperative to know whether and to what extent bivalves will be able to acclimate or adapt to an acidifying ocean over multiple generations. Here, we show that reduced seawater pH projected for the end of this century (i.e., pH 7.7) led to a significant decrease of shell production of newly settled juvenile Manila clams, Ruditapes philippinarum. However, juveniles from parents exposed to low pH grew significantly faster than those from parents grown at ambient pH, exhibiting a rapid transgenerational acclimation to an acidic environment. The sodium composition of the shells may shed new light on the mechanisms responsible for beneficial transgenerational acclimation. Irrespective of parental exposure, the amount of Na incorporated into shells increased with decreasing pH, implying active removal of excessive protons through the Na+/H+ exchanger which is known to depend on the Na+ gradient actively built up by the Na+/K+-ATPase as a driving force. However, the shells with a prior history of transgenerational exposure to low pH recorded significantly lower amounts of Na than those with no history of acidic exposure. It therefore seems very likely that the clams may implement less costly and more ATP-efficient ion regulatory mechanisms to maintain pH homeostasis in the calcifying fluid following transgenerational acclimation. Our results suggest that marine bivalves may have a greater capacity to acclimate or adapt to ocean acidification by the end of this century than currently understood.海洋酸化（Ocean acidification）很可能对海洋双壳类动物（marine bivalves）造成深远影响，尤其会作用于其早期生命阶段。因此，明确双壳类动物能否以及在多大程度上，能够在多代繁衍过程中适应酸化的海洋环境，是一项至关重要的研究课题。本研究表明，本世纪末预测的海水pH降低水平（即pH 7.7）会导致新近附着的菲律宾蛤仔（Ruditapes philippinarum）稚贝的壳形成量显著下降。但亲本曾暴露于低pH环境的稚贝，其生长速度显著快于亲本在正常pH环境下培育的稚贝，表现出对酸性环境的快速跨代适应（transgenerational acclimation）。贝壳的钠元素组成或可为有益跨代适应的作用机制提供新的研究视角。无论亲本是否经历过低pH暴露，贝壳中结合的钠（Na）含量均随pH降低而升高，这意味着机体通过Na+/H+交换蛋白（Na+/H+ exchanger）主动清除过量质子——已知该交换蛋白依赖由Na+/K+-ATP酶（Na+/K+-ATPase）主动建立的钠梯度作为驱动力。但具有跨代低pH暴露历史的贝壳，其钠含量显著低于无酸性暴露历史的贝壳。据此推测，经历跨代适应后，菲律宾蛤仔可能采用了成本更低、ATP利用效率更高的离子调节机制，以维持钙化液（calcifying fluid）中的pH稳态（pH homeostasis）。本研究结果表明，到本世纪末，海洋双壳类动物对海洋酸化的适应能力可能比当前所认知的更强。