Transgenerational biochemical effects of seawater acidification on the Manila clam (Ruditapes philippinarum)

Abstract

Ocean acidification can negatively impact marine bivalves. Pivotal to projecting their fate is the ability to acclimate and adapt to shifts in seawater chemistry. Transgenerational plasticity enables marine bivalves to acclimate, yet the underlying mechanisms at different levels of biological organization remain poorly understood. Here, we performed a transgenerational experiment to understand biochemical responses of the Manila clam, Ruditapes philippinarum, following exposure to moderately reduced seawater pH (from 8.1 to 7.7). Activities of tissue calcification-relevant enzymes, such as carbonic anhydrase (CA), acid phosphatase (ACP) and alkaline phosphatase (ALP), energy-metabolizing enzymes, such as Na+/K+-ATPase (NKA) and Ca2+/Mg2+-ATPase (CMA), as well as tissue energy reserves (glycogen, lipid and protein) were assayed. With decreasing seawater pH, adult R. philippinarum exhibited significantly increased CA activity, and especially the clams with a history of transgenerational exposure displaying significantly higher CA activity than those spawned from parents exposed to ambient seawater pH. Yet, ACP and ALP activities remained unaffected. Transgenerational exposure to reduced seawater pH led to significant increases of NKA activity, while no transgenerational response of CMA activity was observed. Tissue glycogen and lipid contents were significantly depleted under acidified conditions regardless of transgenerational exposure. Yet, transgenerational alleviation in the net protein degradation was found. These findings suggest that our current understanding of transgenerational responses is still limited by the achievable time-window possible in the laboratory. While the energetic budget is lower under acidified conditions, there is no evidence of transgenerational recovery in term of energetic budget. Therefore, this work demonstrates that the critical basis of ocean acidification resilience can most likely be explained in energetic terms.