ABSTRACT
The energetic costs of generating calcium carbonate skeletons and shells in marine organisms remain largely speculative because of the scarcity of empirical data. However, this information is critical for estimating energetic limitations of marine calcifiers that can explain their sensitivity to changes in sea water carbonate chemistry in past, present and future marine systems. Here, the cost of calcification was evaluated using larval stages of the purple sea urchin, Strongylocentrotus purpuratus. We developed a skeleton re-mineralization assay, in which the skeleton was dissolved in live larvae followed by a re-mineralization over a few days. During skeleton re-mineralization, energetic costs were estimated through the measurement of key metabolic parameters including whole-animal metabolic rate, citrate synthase (CS) enzyme activity and mRNA expression as well as mitochondrial density in the calcifying primary mesenchyme cells (PMCs). Minor increases in CS activity and a 10–15% increase in mitochondrial density in PMCs were observed in re-mineralizing larvae as compared with control larvae. Re-mineralization under three different pH conditions (pH 8.1, pH 7.6 and pH 7.1) decreased with decreasing pH, accompanied by pronounced increases in CS expression levels and increased mitochondrial density in PMCs at pH 7.6. Despite a prominent increase in mitochondrial density of primary mesenchyme cells, particularly in the calcifying cohort of this cell type, this work demonstrated a low overall metabolic response to increased mineralization rates at the whole-animal level under both high and low pH conditions. We conclude that calcification in sea urchin larvae is compromised under low pH conditions, associated with low energetic efforts to fuel compensatory processes.
Footnotes
Author contributions
Conceptualization: M.Y.H., T.M.B., S.D., M.S.; Methodology: M.Y.H., T.M.B., W.W.J.C., S.T., F.S., M.S.; Software: M.Y.H., M.S.; Validation: M.Y.H., S.T., F.S., S.D., M.S.; Formal analysis: M.Y.H., W.W.J.C., S.T., S.D., M.S.; Investigation: M.Y.H., T.M.B., W.W.J.C., S.T., F.S.; Resources: M.Y.H., M.S.; Data curation: M.Y.H., M.S.; Writing - original draft: M.Y.H., S.D., M.S.; Writing - review & editing: M.Y.H., T.M.B., W.W.J.C., S.T., S.D., M.S.; Visualization: M.Y.H.; Supervision: M.Y.H., M.S.; Project administration: M.Y.H., M.S.; Funding acquisition: M.Y.H., M.S.
Funding
This work was funded by the Emmy-Noether Programme of the Deutsche Forschungsgemeinschaft (403529967 to M.Y.H. and 441084746 to M.S.). M.Y.H. was co-funded by the European Union (European Research Council, Consolidator grant CarboCell, 101085894). Views and opinions expressed are however those of the author(s) only and do not necessarily reflect those of the European Union or the European Research Council. Neither the European Union nor the granting authority can be held responsible for them. The IAEA is grateful to the Government of the Principality of Monaco for the support provided to its Marine Environment Laboratories.
Data availability
Data are available from the Dryad digital repository (Hu et al., 2024): https://doi.org/10.5061/dryad.gxd2547x4