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

Abstract

The mature skeletons of hard corals, termed stony or scleractinian corals, are made of aragonite (CaCO₃). 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 significantlymore » 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.« less

Authors:

Schmidt, Connor A. ^[1]; Stifler, Cayla A. ^[1]; Luffey, Emily L. ^[1]; Fordyce, Benjamin I. ^[1]; Ahmed, Asiya ^[1]; Barreiro Pujol, Gabriela ^[1]; Breit, Carolyn P. ^[1]; Davison, Sydney S. ^[1]; Klaus, Connor N. ^[1]; Koehler, Isaac J. ^[1]; LeCloux, Isabelle M. ^[1]; Matute Diaz, Celeo ^[1]; Nguyen, Catherine M. ^[1]; Quach, Virginia ^[1]; Sengkhammee, Jaden S. ^[1]; Walch, Evan J. ^[1]; Xiong, Max M. ^[1]; Tambutté, Eric ^[2]; Tambutté, Sylvie ^[2]; Mass, Tali ^[3] more »; Gilbert, Pupa U. P. A.  ^[4]

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+ Show Author Affiliations

1. Department of Physics, University of Wisconsin, Madison, Wisconsin 53706, United States
2. Department of Marine Biology, Centre Scientifique de Monaco, 98000 Monaco, Principality of Monaco
3. Marine Biology Department, University of Haifa, Mt. Carmel, Haifa 31905, Israel
4. Department of Physics, University of Wisconsin, Madison, Wisconsin 53706, United States, Chemical Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, United States, Departments of Chemistry, Materials Science and Engineering, and Geoscience, University of Wisconsin, Madison, Wisconsin 53706, United States

Publication Date:

Mon Jan 17 00:00:00 EST 2022

Research Org.:

Univ. of Wisconsin, Madison, WI (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:

1840626

Alternate Identifier(s):

OSTI ID: 1842276; OSTI ID: 1894064

Grant/Contract Number:  

AC02-05CH11231; FG02-07ER15899

Resource Type:

Published Article

Journal Name:

Journal of the American Chemical Society

Additional Journal Information:

Journal Name: Journal of the American Chemical Society Journal Volume: 144 Journal Issue: 3; Journal ID: ISSN 0002-7863

Publisher:

American Chemical Society

Country of Publication:

United States

Language:

English

Subject:

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Seawater; Vesicles; Crystallization; Nanoparticles; Nucleation