Ocean acidity extremes retard shell formation of bivalve larvae: Insights from transcriptomics and lipidomics

Abstract

In view of climate change and human activities, ocean acidity extreme (OAX) events have been increasingly reported worldwide over the last decades, which possibly retard the growth and development of marine organisms, particularly at their early life-history stages (e.g., embryos or larvae). Thus, understanding whether they can adjust to the sudden increase in seawater acidity has drawn growing attention. Using a commercially and ecologically important bivalve species (Ruditapes philippinarum) with a widespread distribution in the world, we assessed the impact of OAX on its embryonic and larval development as well as expressions of functional genes and lipids to indicate physiological and cellular performance. We found that embryonic development and larval shell formation were inhibited by OAX mainly due to the downregulation of key genes responsible for the uptake of calcium ions from ambient seawater (e.g., NCX, VGCC and SERCA) and the reduced production of bicarbonate ions through the catalytic action of carbonic anhydrase. In addition, a major remodelling in membrane lipids (e.g., PC, PE, PG, PI and PS) indicated that OAX impacted the fluidity and stability of cell membrane, hindering the uptake of calcification substrates. The depletion in energy reserves, such as triacylglycerol, can also account for the impairment in larval shell formation under OAX conditions. By integrating transcriptomics and lipidomics, our findings illustrate a novel molecular mechanism underlying the detrimental effect of OAX on larval development and hence population maintenance of marine organisms, which can have profound implications for sustaining ecosystem stability and aquaculture management.