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Title: Amorphous calcium carbonate particles form coral skeletons

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [2];  [2];  [2];  [3];  [4];  [4];  [4]; ORCiD logo [2]
  1. Univ. of Haifa, Haifa (Israel)
  2. Univ. of Wisconsin-Madison, Madison, WI (United States)
  3. Univ. of Haifa, Haifa (Israel); The Interuniversity Institute of Marine Science, Eilat (Israel)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE
Grant/Contract Number:
AC02-05CH11231; FG02-07ER15899; BSF-2010065; BSF-2014035
OSTI ID:
1377090
Alternate ID(s):
OSTI ID: 1408474
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, Issue 37; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English

References (110)

Cell Biology of Cnidarian-Dinoflagellate Symbiosis journal June 2012
Fossil corals as an archive of secular variations in seawater chemistry since the Mesozoic journal July 2015
Aggregation-Based Crystal Growth and Microstructure Development in Natural Iron Oxyhydroxide Biomineralization Products journal August 2000
Low temperature FESEM of the calcifying interface of a scleractinian coral journal June 2002
Geochemical Perspectives on Coral Mineralization journal January 2003
The Effect of Algal Symbionts on the Accuracy of Sr/Ca Paleotemperatures from Coral journal March 2002
Seawater transport during coral biomineralization journal May 2012
Mesocrystals and Nonclassical Crystallization book January 2008
Solid-State Transformation of Amorphous Calcium Carbonate to Aragonite Captured by CryoTEM journal August 2017
Element partitioning during precipitation of aragonite from seawater: A framework for understanding paleoproxies journal September 2006
Coral Calcification, Cells to Reefs book November 2010
Sr/Ca and Mg/Ca vital effects correlated with skeletal architecture in a scleractinian deep-sea coral and the role of Rayleigh fractionation journal September 2007
Correlation of boron isotopic composition with ultrastructure in the deep-sea coral Lophelia pertusa : Implications for biomineralization and paleo-pH : BORON ISOTOPIC COMPOSITION IN CORAL journal December 2007
Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification journal May 2011
The incorporation of Mg2+ and Sr2+ into calcite overgrowths: influences of growth rate and solution composition journal February 1983
The Geological Record of Ocean Acidification text January 2012
Studies of the growth and dissolution kinetics of the CaCO3 polymorphs calcite and aragonite I. Growth and dissolution rates in water journal January 1996
Mollusk Shell Nacre Ultrastructure Correlates with Environmental Temperature and Pressure journal March 2012
Narrowly Distributed Crystal Orientation in Biomineral Vaterite journal September 2015
Hierarchical Control of Lymphocyte Survival journal October 1996
A New Coral Carbonic Anhydrase in Stylophora pistillata journal February 2011
Accelerated thawing of subarctic peatland permafrost over the last 50 years journal January 2004
Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms text January 2005
Coral biomineralization: From the gene to the environment journal November 2011
Observations of the tissue-skeleton interface in the scleractinian coral Stylophora pistillata journal June 2007
Biomineral nanoparticles are space-filling journal January 2011
Immunolocalization of skeletal matrix proteins in tissue and mineral of the coral Stylophora pistillata journal August 2014
Peptides Enhance Magnesium Signature in Calcite: Insights into Origins of Vital Effects journal October 2008
Initial stages of calcium uptake and mineral deposition in sea urchin embryos journal December 2013
Transformation and crystallization energetics of synthetic and biogenic amorphous calcium carbonate journal September 2010
Measurement of c-axis angular orientation in calcite (CaCO3) nanocrystals using X-ray absorption spectroscopy journal June 2011
Energetic clues to pathways to biomineralization: Precursors, clusters, and nanoparticles journal August 2004
Relative precipitation rates of aragonite and Mg calcite from seawater: Temperature or carbonate ion control? journal January 1987
Oxygen Spectroscopy and Polarization-Dependent Imaging Contrast (PIC)-Mapping of Calcium Carbonate Minerals and Biominerals journal May 2014
Skeletal mineralogy of newly settling Acropora millepora (Scleractinia) coral recruits journal September 2010
Branch to colony trajectory in a modular organism: Pattern formation in the Indo-Pacific coralStylophora pistillata journal January 2006
Photoacclimation of Stylophora pistillata to light extremes: metabolism and calcification journal March 2007
Compensation of charging in X-PEEM: a successful test on mineral inclusions in 4.4Ga old zircon journal December 2003
Mechanism of Calcite Co-Orientation in the Sea Urchin Tooth journal December 2009
Mineral-bearing vesicle transport in sea urchin embryos journal December 2015
Effect of seawater carbonate concentration on foraminiferal carbon and oxygen isotopes journal December 1997
Phase transitions in biogenic amorphous calcium carbonate journal April 2012
Morphology development and crystal growth in nanocrystalline aggregates under hydrothermal conditions: insights from titania journal May 1999
The crystallization of calcium carbonate. II. Calcite growth mechanism journal December 1971
Coral calcifying fluid pH is modulated by seawater carbonate chemistry not solely seawater pH journal January 2017
The composition of Standard Seawater and the definition of the Reference-Composition Salinity Scale journal January 2008
Nanoscale Transforming Mineral Phases in Fresh Nacre journal October 2015
In vivo light-microscopic documentation for primary calcification processes in the hermatypic coral Stylophora pistillata journal March 2006
Ocean acidification causes bleaching and productivity loss in coral reef builders journal November 2008
Particle Accretion Mechanism Underlies Biological Crystal Growth from an Amorphous Precursor Phase journal July 2014
Effects on growth and reproduction of the coral Stylophora pistillata by the mutualistic damselfish Dascyllus marginatus journal February 1995
Calcium transport into the cells of the sea urchin larva in relation to spicule formation journal October 2016
Sea-Surface Temperature from Coral Skeletal Strontium/Calcium Ratios journal July 1992
Mesocrystals: Inorganic Superstructures Made by Highly Parallel Crystallization and Controlled Alignment journal November 2005
Sea Urchin Spine Calcite Forms via a Transient Amorphous Calcium Carbonate Phase journal November 2004
The solubility of calcite and aragonite in seawater of 35%. salinity at 25°C and atmospheric pressure journal January 1980
Architecture of Columnar Nacre, and Implications for Its Formation Mechanism journal June 2007
Crystallization by particle attachment in synthetic, biogenic, and geologic environments journal July 2015
Global warming and recurrent mass bleaching of corals journal March 2017
Calcite and aragonite precipitation from seawater solutions of various salinities: Precipitation rates and overgrowth compositions journal December 1989
PALEOCLIMATE: Corals, Chemistry, and Climate journal April 2002
Imaging intracellular pH in a reef coral and symbiotic anemone journal August 2009
Biomineralization in Mediterranean Corals: The Role of the Intraskeletal Organic Matrix journal July 2014
The Geological Record of Ocean Acidification journal March 2012
Amorphous calcium carbonate transforms into calcite during sea urchin larval spicule growth journal March 1997
Polarization-dependent imaging contrast in abalone shells journal February 2008
Asprich Peptides Are Occluded in Calcite and Permanently Disorder Biomineral Crystals journal August 2010
An Overview of Biomineralization Processes and the Problem of the Vital Effect journal January 2003
Rapid Acidification of the Ocean During the Paleocene-Eocene Thermal Maximum journal June 2005
Biomineralization pathways in a foraminifer revealed using a novel correlative cryo-fluorescence–SEM–EDS technique journal November 2016
Crystal nucleation and near-epitaxial growth in nacre journal December 2013
Study of calcification during a daily cycle of the coral Stylophora pistillata: implications for `light-enhanced calcification' journal September 2006
Coral biomineralization: A focus on intra-skeletal organic matrix and calcification journal October 2015
Implication of water depth on stable isotope composition and skeletal density banding patterns in a Porites lutea colony: results from a long-term translocation experiment journal December 2003
Solid-State Transformation of Amorphous Calcium Carbonate to Aragonite Captured by CryoTEM journal August 2017
Coral Skeleton Construction: A Physiochemically Dominated Process journal April 1986
Calcium Carbonate Polyamorphism and Its Role in Biomineralization: How Many Amorphous Calcium Carbonates Are There? journal November 2012
Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite journal August 2002
13C–18O bonds in carbonate minerals: A new kind of paleothermometer journal March 2006
XANES mapping of organic sulfate in three scleractinian coral skeletons journal January 2003
A proteinaceous organic matrix regulates carbonate mineral production in the marine teleost intestine journal October 2016
Kinetic control of skeletal Sr/Ca in a symbiotic coral: Implications for the paleotemperature proxy journal February 2001
Spherulitic Growth of Coral Skeletons and Synthetic Aragonite: Nature’s Three-Dimensional Printing journal June 2017
Water as the Key to Proto-Aragonite Amorphous CaCO 3 journal June 2016
A Non-traditional Stable Isotope Perspective on Coral Calcification book January 2016
Incorporation of Metabolic CO2 into Coral Skeleton journal October 1970
Coccolith Sr/Ca as a new indicator of coccolithophorid calcification and growth rate: COCCOLITH Sr/Ca journal May 2000
The Ostwald step rule journal November 1984
Stable isotopes in deep-sea corals and a new mechanism for “vital effects” journal March 2003
The solubility of calcite and aragonite in sulfate-free seawater and the seeded growth kinetics and composition of the precipitates at 25°C journal January 1989
Live Tissue Imaging Shows Reef Corals Elevate pH under Their Calcifying Tissue Relative to Seawater journal May 2011
Biomineralization in newly settled recruits of the scleractinian coral Pocillopora damicornis : Biomineralization in journal June 2014
Controls on magnesium and strontium uptake in planktonic foraminifera determined by live culturing journal August 1999
The 27-year decline of coral cover on the Great Barrier Reef and its causes journal October 2012
Comparative genomics explains the evolutionary success of reef-forming corals journal May 2016
Mesocrystals: Inorganic Superstructures Made by Highly Parallel Crystallization and Controlled Alignment journal September 2005
Growth Rates of Three Reef-Building Coral Species in the Northern red sea, Egypt journal September 2001
Biological control of aragonite formation in stony corals journal June 2017
Bicarbonate transporters in corals point towards a key step in the evolution of cnidarian calcification journal June 2015
The probing depth of total electron yield in the sub-keV range: TEY-XAS and X-PEEM journal July 2003
Effects of particulate matter released by a fish farm (Eilat, Red Sea) on survival and growth of Stylophora pistillata coral nubbins journal September 2003
Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms journal September 2005
Transformation mechanism of amorphous calcium carbonate into calcite in the sea urchin larval spicule journal November 2008
Measurement of Paleotemperatures and Temperatures of the Upper Cretaceous of England, Denmark, and the Southeastern United States journal January 1951
On Biomineralization book July 1989
Distribution of magnesium in coral skeleton: MG MICRODISTRIBUTION IN CORAL journal December 2004
A compartmental approach to the mechanism of calcification in hermatypic corals journal May 1996
Photoemission spectromicroscopy for the biomineralogist book February 2014
Control of Aragonite or Calcite Polymorphism by Mollusk Shell Macromolecules journal January 1996
Calcium Carbonate Polyamorphism and Its Role in Biomineralization: How Many Amorphous Calcium Carbonates Are There? text January 2012

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