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）可能对海洋双壳类（marine bivalves）产生深远影响，尤其会作用于其早期生活史阶段。因此，明确双壳类能否以及在多大程度上可在多世代尺度下适应酸化海洋，是一项亟需开展的研究。本研究显示，本世纪末预估的海水pH降低水平（即pH 7.7）会显著降低新近附着的菲律宾蛤仔（Manila clam, Ruditapes philippinarum）稚贝的贝壳形成量。然而，亲代暴露于低pH环境下产生的稚贝，其生长速度显著快于亲代在环境pH下培育的稚贝，表现出对酸性环境的快速跨世代驯化。贝壳的钠元素组成或可为阐明有益跨世代驯化的机制提供新视角。无论亲代是否经历过低pH暴露，贝壳中结合的钠含量均随pH降低而升高，这意味着生物可通过钠氢交换蛋白（Na+/H+ exchanger）主动清除过量质子——已知该交换蛋白依赖钠钾ATP酶（Na+/K+-ATPase）主动建立的钠梯度作为驱动力。但具有跨世代低pH暴露史的稚贝贝壳，其钠含量显著低于无酸性暴露史的稚贝贝壳。由此推测，经历跨世代驯化后，菲律宾蛤仔可能会采用成本更低、ATP利用效率更高的离子调控机制，以维持钙化液中的pH稳态。本研究结果表明，海洋双壳类对本世纪末海洋酸化的适应或驯化能力，可能远超当前的认知水平。