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Title: Biomineralization by particle attachment in early animals

Abstract

Crystallization by particle attachment (CPA) of amorphous precursors has been demonstrated in modern biomineralized skeletons across a broad phylogenetic range of animals. Precisely the same precursors, hydrated (ACC-H 2 O) and anhydrous calcium carbonate (ACC), have been observed spectromicroscopically in echinoderms, mollusks, and cnidarians, phyla drawn from the 3 major clades of eumetazoans. Scanning electron microscopy (SEM) here also shows evidence of CPA in tunicate chordates. This is surprising, as species in these clades have no common ancestor that formed a mineralized skeleton and appear to have evolved carbonate biomineralization independently millions of years after their late Neoproterozoic divergence. Here we correlate the occurrence of CPA from ACC precursor particles with nanoparticulate fabric and then use the latter to investigate the antiquity of the former. SEM images of early biominerals from Ediacaran and Cambrian shelly fossils show that these early calcifiers used attachment of ACC particles to form their biominerals. The convergent evolution of biomineral CPA may have been dictated by the same thermodynamics and kinetics as we observe today.

Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1557898
Alternate Identifier(s):
OSTI ID: 1609805
Grant/Contract Number:  
FG02-07ER15899
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 36; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & Technology

Citation Formats

Biomineralization by particle attachment in early animals. United States: N. p., 2019. Web. doi:10.1073/pnas.1902273116.
Biomineralization by particle attachment in early animals. United States. https://doi.org/10.1073/pnas.1902273116
Mon . "Biomineralization by particle attachment in early animals". United States. https://doi.org/10.1073/pnas.1902273116.
@article{osti_1557898,
title = {Biomineralization by particle attachment in early animals},
author = {None, None},
abstractNote = {Crystallization by particle attachment (CPA) of amorphous precursors has been demonstrated in modern biomineralized skeletons across a broad phylogenetic range of animals. Precisely the same precursors, hydrated (ACC-H 2 O) and anhydrous calcium carbonate (ACC), have been observed spectromicroscopically in echinoderms, mollusks, and cnidarians, phyla drawn from the 3 major clades of eumetazoans. Scanning electron microscopy (SEM) here also shows evidence of CPA in tunicate chordates. This is surprising, as species in these clades have no common ancestor that formed a mineralized skeleton and appear to have evolved carbonate biomineralization independently millions of years after their late Neoproterozoic divergence. Here we correlate the occurrence of CPA from ACC precursor particles with nanoparticulate fabric and then use the latter to investigate the antiquity of the former. SEM images of early biominerals from Ediacaran and Cambrian shelly fossils show that these early calcifiers used attachment of ACC particles to form their biominerals. The convergent evolution of biomineral CPA may have been dictated by the same thermodynamics and kinetics as we observe today.},
doi = {10.1073/pnas.1902273116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 36,
volume = 116,
place = {United States},
year = {Mon Aug 19 00:00:00 EDT 2019},
month = {Mon Aug 19 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1073/pnas.1902273116

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Works referenced in this record:

Particle Accretion Mechanism Underlies Biological Crystal Growth from an Amorphous Precursor Phase
journal, July 2014

  • Gal, Assaf; Kahil, Keren; Vidavsky, Netta
  • Advanced Functional Materials, Vol. 24, Issue 34
  • DOI: 10.1002/adfm.201400676

Transformation and crystallization energetics of synthetic and biogenic amorphous calcium carbonate
journal, September 2010

  • Radha, A. V.; Forbes, T. Z.; Killian, C. E.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 38
  • DOI: 10.1073/pnas.1009959107

Uncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales
journal, November 2015

  • dos Reis, Mario; Thawornwattana, Yuttapong; Angelis, Konstantinos
  • Current Biology, Vol. 25, Issue 22
  • DOI: 10.1016/j.cub.2015.09.066

Amorphous Calcium Carbonate is Stabilized in Confinement
journal, June 2010

  • Stephens, Christopher J.; Ladden, Sophie F.; Meldrum, Fiona C.
  • Advanced Functional Materials, Vol. 20, Issue 13
  • DOI: 10.1002/adfm.201000248

Sea Urchin Spine Calcite Forms via a Transient Amorphous Calcium Carbonate Phase
journal, November 2004


Shape-preserving transformation of carbonate minerals into lead halide perovskite semiconductors based on ion exchange/insertion reactions
journal, June 2018


A stem-group cnidarian described from the mid-Cambrian of China and its significance for cnidarian evolution
journal, August 2011

  • Park, Tae-yoon; Woo, Jusun; Lee, Dong-Jin
  • Nature Communications, Vol. 2, Issue 1
  • DOI: 10.1038/ncomms1457

Chronology of early Cambrian biomineralization
journal, August 2011


Crystallization by particle attachment in synthetic, biogenic, and geologic environments
journal, July 2015

  • De Yoreo, J. J.; Gilbert, P. U. P. A.; Sommerdijk, N. A. J. M.
  • Science, Vol. 349, Issue 6247
  • DOI: 10.1126/science.aaa6760

Halkieriids in Middle Cambrian Phosphatic Limestones from Australia
journal, May 2004


Crystallographic control on the substructure of nacre tablets
journal, September 2013

  • Checa, Antonio G.; Mutvei, Harry; Osuna-Mascaró, Antonio J.
  • Journal of Structural Biology, Vol. 183, Issue 3
  • DOI: 10.1016/j.jsb.2013.07.014

Analogous biomineralization processes between the fossil coral Calceola sandalina (Rugosa, Devonian) and other Recent and fossil cnidarians
journal, November 2016

  • Coronado, Ismael; Pérez-Huerta, Alberto; Rodríguez, Sergio
  • Journal of Structural Biology, Vol. 196, Issue 2
  • DOI: 10.1016/j.jsb.2016.06.013

Amorphous calcium phosphate is a major component of the forming fin bones of zebrafish: Indications for an amorphous precursor phase
journal, August 2008

  • Mahamid, J.; Sharir, A.; Addadi, L.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 35
  • DOI: 10.1073/pnas.0803354105

Nacre tablet thickness records formation temperature in modern and fossil shells
journal, February 2017

  • Gilbert, Pupa U. P. A.; Bergmann, Kristin D.; Myers, Corinne E.
  • Earth and Planetary Science Letters, Vol. 460
  • DOI: 10.1016/j.epsl.2016.11.012

The Cambrian Conundrum: Early Divergence and Later Ecological Success in the Early History of Animals
journal, November 2011


Amorphous calcium carbonate particles form coral skeletons
journal, August 2017

  • Mass, Tali; Giuffre, Anthony J.; Sun, Chang-Yu
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 37
  • DOI: 10.1073/pnas.1707890114

Biomineralization and Evolutionary History
journal, January 2003

  • Knoll, A. H.
  • Reviews in Mineralogy and Geochemistry, Vol. 54, Issue 1
  • DOI: 10.2113/0540329

Amorphous calcium carbonate transforms into calcite during sea urchin larval spicule growth
journal, March 1997

  • Beniash, Elia; Aizenberg, Joanna; Addadi, Lia
  • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 264, Issue 1380
  • DOI: 10.1098/rspb.1997.0066

Transient amorphous calcium phosphate in forming enamel
journal, May 2009

  • Beniash, Elia; Metzler, Rebecca A.; Lam, Raymond S. K.
  • Journal of Structural Biology, Vol. 166, Issue 2
  • DOI: 10.1016/j.jsb.2009.02.001

Water: How Does It Influence the CaCO 3 Formation?
journal, November 2019


Oriented attachment and growth, twinning, polytypism, and formation of metastable phases; insights from nanocrystalline TiO 2
journal, October 1998


Skeletal Microstructure Indicates Chancelloriids and Halkieriids are Closely Related
journal, July 2008


Narrowly Distributed Crystal Orientation in Biomineral Vaterite
journal, September 2015


Calcified metazoans in thrombolite-stromatolite reefs of the terminal Proterozoic Nama Group, Namibia
journal, September 2000


New animal phylogeny: future challenges for animal phylogeny in the age of phylogenomics
journal, September 2015


Self-Sharpening Mechanism of the Sea Urchin Tooth
journal, December 2010

  • Killian, Christopher E.; Metzler, Rebecca A.; Gong, Yutao
  • Advanced Functional Materials, Vol. 21, Issue 4
  • DOI: 10.1002/adfm.201001546

Revealing crystalline domains in a mollusc shell single-crystalline prism
journal, July 2017

  • Mastropietro, F.; Godard, P.; Burghammer, M.
  • Nature Materials, Vol. 16, Issue 9
  • DOI: 10.1038/nmat4937

Engineering Porosity into Single-Crystal Colloidal Nanosheets Using Epitaxial Nucleation and Chalcogenide Anion Exchange Reactions: The Conversion of SnSe to SnTe
journal, July 2012

  • Sines, Ian T.; Vaughn, Dimitri D.; Biacchi, Adam J.
  • Chemistry of Materials, Vol. 24, Issue 15
  • DOI: 10.1021/cm301734b

Evolutionary Origins of Animal Skeletal Biomineralization
journal, January 2011

  • Murdock, Duncan J. E.; Donoghue, Philip C. J.
  • Cells Tissues Organs, Vol. 194, Issue 2-4
  • DOI: 10.1159/000324245

New data on molluscs and their shell microstructures from the Middle Cambrian Gowers Formation, Australia
journal, January 2010


Cation Exchange Reactions in Ionic Nanocrystals
journal, November 2004

  • Son, Dong Hee; Hughes, Steven M.; Yin, Yadong
  • Science, Vol. 306, Issue 5698, p. 1009-1012
  • DOI: 10.1126/science.1103755

Sequential Anion and Cation Exchange Reactions for Complete Material Transformations of Nanoparticles with Morphological Retention
journal, June 2015

  • Hodges, James M.; Kletetschka, Karel; Fenton, Julie L.
  • Angewandte Chemie International Edition, Vol. 54, Issue 30
  • DOI: 10.1002/anie.201504099

Life history and autecology of an Ediacaran index fossil: Development and dispersal of Cloudina
journal, August 2015


Mechanism of Calcite Co-Orientation in the Sea Urchin Tooth
journal, December 2009

  • Killian, Christopher E.; Metzler, Rebecca A.; Gong, Y. U. T.
  • Journal of the American Chemical Society, Vol. 131, Issue 51
  • DOI: 10.1021/ja907063z

Shell microstructures of Cambrian molluscs replicated by phosphate
journal, January 1985


Phase transitions in biogenic amorphous calcium carbonate
journal, April 2012

  • Gong, Y. U. T.; Killian, C. E.; Olson, I. C.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 16
  • DOI: 10.1073/pnas.1118085109

Transformation mechanism of amorphous calcium carbonate into calcite in the sea urchin larval spicule
journal, November 2008

  • Politi, Y.; Metzler, R. A.; Abrecht, M.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 45
  • DOI: 10.1073/pnas.0806604105

Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite
journal, August 2002

  • Weiss, Ingrid Maria; Tuross, Noreen; Addadi, Lia
  • Journal of Experimental Zoology, Vol. 293, Issue 5
  • DOI: 10.1002/jez.90004

Nanoscale Transforming Mineral Phases in Fresh Nacre
journal, October 2015

  • DeVol, Ross T.; Sun, Chang-Yu; Marcus, Matthew A.
  • Journal of the American Chemical Society, Vol. 137, Issue 41
  • DOI: 10.1021/jacs.5b07931

Crystallization kinetics of amorphous calcium carbonate in confinement
journal, January 2019

  • Cavanaugh, Jack; Whittaker, Michael L.; Joester, Derk
  • Chemical Science, Vol. 10, Issue 19
  • DOI: 10.1039/C8SC05634J