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Research Article

Amorphous calcium carbonate particles form coral skeletons

Tali Mass, Anthony J. Giuffre, Chang-Yu Sun, Cayla A. Stifler, Matthew J. Frazier, Maayan Neder, Nobumichi Tamura, Camelia V. Stan, Matthew A. Marcus, and View ORCID ProfilePupa U. P. A. Gilbert
PNAS first published August 28, 2017; https://doi.org/10.1073/pnas.1707890114
Tali Mass
aMarine Biology Department, University of Haifa, Haifa 31905, Israel;
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  • For correspondence: tmass@univ.haifa.ac.il pupa@physics.wisc.edu
Anthony J. Giuffre
bDepartment of Physics, University of Wisconsin–Madison, Madison, WI 53706;
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Chang-Yu Sun
bDepartment of Physics, University of Wisconsin–Madison, Madison, WI 53706;
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Cayla A. Stifler
bDepartment of Physics, University of Wisconsin–Madison, Madison, WI 53706;
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Matthew J. Frazier
bDepartment of Physics, University of Wisconsin–Madison, Madison, WI 53706;
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Maayan Neder
aMarine Biology Department, University of Haifa, Haifa 31905, Israel;
cH. Steinitz Marine Biology Laboratory, The Interuniversity Institute of Marine Science, Eilat 88103, Israel;
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Nobumichi Tamura
dAdvanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA 94720;
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Camelia V. Stan
dAdvanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA 94720;
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Matthew A. Marcus
dAdvanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA 94720;
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Pupa U. P. A. Gilbert
bDepartment of Physics, University of Wisconsin–Madison, Madison, WI 53706;
eDepartment of Chemistry, University of Wisconsin–Madison, Madison, WI 53706;
fDepartment of Geoscience, University of Wisconsin–Madison, Madison, WI 53706
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  • ORCID record for Pupa U. P. A. Gilbert
  • For correspondence: tmass@univ.haifa.ac.il pupa@physics.wisc.edu
  1. Edited by Andrew H. Knoll, Harvard University, Cambridge, MA, and approved July 28, 2017 (received for review May 15, 2017)

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Significance

Whether coral skeleton crystals grow by attachment of ions from solution or particles from tissue determines (i) corals’ growth rate, (ii) how they survive acidifying oceans, and (iii) the isotopes in the crystals used for reconstructing ancient temperatures. Our data show that two amorphous precursors exist, one hydrated and one dehydrated amorphous calcium carbonate; that these are formed in the tissue as ∼400-nm particles; and that they attach to the surface of coral skeletons, remain amorphous for hours, and finally crystallize into aragonite. Since these particles are formed inside tissue, coral skeleton growth may be less susceptible to ocean acidification than previously assumed. Coral bleaching and postmortem dissolution of the skeleton will occur, but a calcification crisis may not.

Abstract

Do corals form their skeletons by precipitation from solution or by attachment of amorphous precursor particles as observed in other minerals and biominerals? The classical model assumes precipitation in contrast with observed “vital effects,” that is, deviations from elemental and isotopic compositions at thermodynamic equilibrium. Here, we show direct spectromicroscopy evidence in Stylophora pistillata corals that two amorphous precursors exist, one hydrated and one anhydrous amorphous calcium carbonate (ACC); that these are formed in the tissue as 400-nm particles; and that they attach to the surface of coral skeletons, remain amorphous for hours, and finally, crystallize into aragonite (CaCO3). We show in both coral and synthetic aragonite spherulites that crystal growth by attachment of ACC particles is more than 100 times faster than ion-by-ion growth from solution. Fast growth provides a distinct physiological advantage to corals in the rigors of the reef, a crowded and fiercely competitive ecosystem. Corals are affected by warming-induced bleaching and postmortem dissolution, but the finding here that ACC particles are formed inside tissue may make coral skeleton formation less susceptible to ocean acidification than previously assumed. If this is how other corals form their skeletons, perhaps this is how a few corals survived past CO2 increases, such as the Paleocene–Eocene Thermal Maximum that occurred 56 Mya.

  • mesocrystal
  • PEEM
  • calcification crisis
  • vital effects
  • ocean acidification

Footnotes

  • ↵1To whom correspondence may be addressed. Email: tmass{at}univ.haifa.ac.il or pupa{at}physics.wisc.edu.
  • ↵2Previously publishing as Gelsomina De Stasio.

  • Author contributions: P.U.P.A.G. designed research; T.M., A.J.G., C.-Y.S., M.N., N.T., C.V.S., and P.U.P.A.G. performed research; T.M. and M.J.F. contributed new reagents/analytic tools; A.J.G., C.-Y.S., C.A.S., N.T., M.A.M., and P.U.P.A.G. analyzed data; and P.U.P.A.G. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1707890114/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Growing coral crystals attach particles, not ions
Tali Mass, Anthony J. Giuffre, Chang-Yu Sun, Cayla A. Stifler, Matthew J. Frazier, Maayan Neder, Nobumichi Tamura, Camelia V. Stan, Matthew A. Marcus, Pupa U. P. A. Gilbert
Proceedings of the National Academy of Sciences Aug 2017, 201707890; DOI: 10.1073/pnas.1707890114

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Growing coral crystals attach particles, not ions
Tali Mass, Anthony J. Giuffre, Chang-Yu Sun, Cayla A. Stifler, Matthew J. Frazier, Maayan Neder, Nobumichi Tamura, Camelia V. Stan, Matthew A. Marcus, Pupa U. P. A. Gilbert
Proceedings of the National Academy of Sciences Aug 2017, 201707890; DOI: 10.1073/pnas.1707890114
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