Faster Crystallization during Coral Skeleton Formation Correlates with Resilience to Ocean Acidification

• Main Authors: Connor A. Schmidt (11955321), Cayla A. Stifler (4592338), Emily L. Luffey (11955324), Benjamin I. Fordyce (11955327), Asiya Ahmed (11955330), Gabriela Barreiro Pujol (11955333), Carolyn P. Breit (11955336), Sydney S. Davison (11955339), Connor N. Klaus (11955342), Isaac J. Koehler (11955345), Isabelle M. LeCloux (11955348), Celeo Matute Diaz (11955351), Catherine M. Nguyen (6640097), Virginia Quach (5905445), Jaden S. Sengkhammee (11955354), Evan J. Walch (11955357), Max M. Xiong (11955360), Eric Tambutté (4400305), Sylvie Tambutté (11955363), Tali Mass (103384), Pupa U. P. A. Gilbert (11507551)
• Format: Other Non-Article Part of Journal/Newspaper
• Language: unknown
• Published: 2022
• Subjects: Physiology; Evolutionary Biology; Ecology; Inorganic Chemistry; Environmental Sciences not elsewhere classified; Chemical Sciences not elsewhere classified; three diverse genera; thickness across genera; extracellular calcifying fluid; > differently sensitive; amorphous precursor phases; >; whose response; turbinaria peltata </; stylophora pistillata </; turbinaria </; stylophora </; acropora </; transiently amorphous; amorphous particles; termed stony; sp .; soluble longer; previously assumed; present data; partly open; particle attachment; ocean acidification; observed frequently; mature skeletons; major source; intracellular vesicles; including overnight; growing surface; gradually crystallize; formed away; faster crystallization; coral skeletons; closed vesicles; calcium carbonate; additive manufacturing; demonstrating; based; 9 μm; Ocean acidification
• Online Access: https://doi.org/10.1021/jacs.1c11434.s001

The mature skeletons of hard corals, termed stony or scler­actin­ian corals, are made of aragonite (CaCO 3 ). During their formation, particles attaching to the skeleton’s growing surface are calcium carbonate, transiently amorphous. Here we show that amorphous particles are observed frequently and reproducibly just outside the skeleton, where a calico­blastic cell layer envelops and deposits the forming skeleton. The observation of particles in these locations, therefore, is consistent with nucleation and growth of particles in intracellular vesicles. The observed extraskeletal particles range in size between 0.2 and 1.0 μm and contain more of the amorphous precursor phases than the skeleton surface or bulk, where they gradually crystallize to aragonite. This observation was repeated in three diverse genera of corals, Acropora sp., Stylophora pistillata differently sensitive to ocean acidification (OA)and Turbinaria peltata , demonstrating that intracellular particles are a major source of material during the additive manufacturing of coral skeletons. Thus, particles are formed away from seawater, in a presumed intracellular calcifying fluid (ICF) in closed vesicles and not, as previously assumed, in the extracellular calcifying fluid (ECF), which, unlike ICF, is partly open to seawater. After particle attachment, the growing skeleton surface remains exposed to ECF, and, remarkably, its crystallization rate varies significantly across genera. The skeleton surface layers containing amorphous pixels vary in thickness across genera: ∼2.1 μm in Acropora , 1.1 μm in Stylophora , and 0.9 μm in Turbinaria . Thus, the slow-crystallizing Acropora skeleton surface remains amorphous and soluble longer, including overnight, when the pH in the ECF drops. Increased skeleton surface solubility is consistent with Acropora ’s vulnerability to OA, whereas the Stylophora skeleton surface layer crystallizes faster, consistent with Stylophora ’s resilience to OA. Turbinaria , whose response to OA has not yet been tested, is expected to be even more resilient than Stylophora , based on the present data.