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Transformation Mechanism of Amorphous Calcium Carbonate Into Calcite in the Sea Urchin Larval Spicule

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Transformation Mechanism of Amorphous Calcium Carbonate Into Calcite in the Sea Urchin Larval Spicule NEUROSCIENCE. For the article ‘‘Rapid enhancement of two-step APPLIED BIOLOGICAL SCIENCES. For the article ‘‘Accurately quanti- wiring plasticity by estrogen and NMDA receptor activity,’’ by fying low-abundant targets amid similar sequences by revealing Deepak P. Srivastava, Kevin Woolfrey, Kelly A. Jones, Cassan- hidden correlations in oligonucleotide microarray data,’’ by dra Y. Shum, L. Leanne Lash, Geoffrey T. Swanson, and Peter Luisa A. Marcelino, Vadim Backman, Andres Donaldson, Clau- Penzes, which appeared in issue 38, September 23, 2008, of Proc dia Steadman, Janelle R. Thompson, Sarah Pacocha Preheim, Natl Acad Sci USA (105:14650–14655; first published September Cynthia Lien, Eelin Lim, Daniele Veneziano, and Martin F. 18, 2008; 10.1073͞pnas.0801581105), the authors note that the Polz, which appeared in issue 37, September 12, 2006, of Proc author name Kevin Woolfrey should have appeared as Kevin M. Natl Acad Sci USA (103:13629–13634; first published September Woolfrey. The author line has been corrected online. In addition, 1, 2006; 10.1073͞pnas.0601476103), the authors note that in Eq. in the author contributions footnote and in the Acknowledg- 4,aϪ1 was inadvertently omitted from the denominator. The ments, the initials K.W. should appear as K.M.W. The authors data in Fig. 1 were calculated using the correct equation, and this also note that due to a printer’s error, in Fig. 3A, some colors error in the published equation would make Ͻ1% difference in printed incorrectly. The corrected author line, and the corrected the values of ␤. The corrected equation appears below. figure and its legend, appear below. 1 1 Deepak P. Srivastava, Kevin M. Woolfrey, Kelly A. Jones, ␤ ϭ Ϫ jk 1 ⌬ , [4] b Gjk Cassandra Y. Shum, L. Leanne Lash, Geoffrey T. Swanson, ΂ Ϫ2 hͩ Ϫ1ͪ΃ ͱ ϩ ͩ͑ Ϫ ͒ Ϫ ͪ ⌬ 1 1 b 1 e Gjj and Peter Penzes www.pnas.org͞cgi͞doi͞10.1073͞pnas.0809790105 BIOPHYSICS, CHEMISTRY. For the article ‘‘Transformation mecha- nism of amorphous calcium carbonate into calcite in the sea urchin larval spicule,’’ by Yael Politi, Rebecca A. Metzler, Mike Abrecht, Benjamin Gilbert, Fred H. Wilt, Irit Sagi, Lia Addadi, Steve Weiner, and Pupa Gilbert, which appeared in issue 45, November 11, 2008, of Proc Natl Acad Sci USA (105:17362– 17366; first published November 5, 2008; 10.1073͞pnas. 0806604105), the authors note that the author name Pupa Gilbert should have appeared as P. U. P. A. Gilbert. The author line has been corrected online. In addition, in the author contributions footnote and in the Acknowledgments, the initials P.G. should appear as P.U.P.A.G. The corrected author line appears below. Yael Politi, Rebecca A. Metzler, Mike Abrecht, Benjamin Gilbert, Fred H. Wilt, Irit Sagi, Lia Addadi, Steve Weiner, and P. U. P. A. Gilbert www.pnas.org͞cgi͞doi͞10.1073͞pnas.0811530106 CORRECTIONS Fig. 3. E2 rapidly and transiently induces the formation of silent synapses through trafficking of GluR1 and NR1. (A and B) Time-lapse imaging of neurons expressing GFP-GluR1. Cells were imaged for 60 min before and after administration of E2. Arrowheads indicate GFP-GluR1 in spine heads; arrows indicate GFP-GluR1 in dendritic shaft. Dotted lines indicate neuron outline, as determined by Discosoma red fluorescent protein coexpression; asterisks show transient emergence of novel spines upon E2 treatment. (Scale bars, 1 ␮m.) (C) AMPAR mEPSCs after E2 treatment. Frequency and average ampli- tude of mEPSCs were measured; frequency, but not amplitude, of mEPSCs was significantly reduced at 30 min. *, P Ͻ 0.05; ***, P Ͻ 0.001. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0810024105 PNAS ͉ December 16, 2008 ͉ vol. 105 ͉ no. 50 ͉ 20045 Downloaded by guest on September 25, 2021 Transformation mechanism of amorphous calcium carbonate into calcite in the sea urchin larval spicule Yael Politia, Rebecca A. Metzlerb, Mike Abrechtc, Benjamin Gilbertd, Fred H. Wilte, Irit Sagia, Lia Addadia,1, Steve Weinera,1, and P. U. P. A. Gilbertb,1,2 aDepartment of Structural Biology, Weizmann Institute of Science, Rehovot 76100, Israel; bDepartment of Physics, University of Wisconsin, Madison, WI 53706; cSynchrotron Radiation Center, Stoughton, WI 53589; dEarth Science Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720; and eDepartment of Molecular and Cell Biology, University of California, Berkeley, CA 94720-3200 Edited by Jack Halpern, University of Chicago, Chicago, IL, and approved September 25, 2008 (received for review July 8, 2008) Sea urchin larval spicules transform amorphous calcium carbonate is composed of densely packed mineral spherules 40–100 nm (ACC) into calcite single crystals. The mechanism of transformation in diameter (3, 17). No crystallization front can be detected at is enigmatic: the transforming spicule displays both amorphous the micrometer scale. Extended X-ray absorption fine structure and crystalline properties, with no defined crystallization front. (EXAFS) spectroscopy at the Ca K-edge showed that even at Here, we use X-ray photoelectron emission spectromicroscopy early stages, when the mineral is still predominantly amorphous, with probing size of 40–200 nm. We resolve 3 distinct mineral it already has a nascent short-range order around the calcium phases: An initial short-lived, presumably hydrated ACC phase, ions similar to that in calcite (18). In contrast to stable biogenic followed by an intermediate transient form of ACC, and finally the ACC, which contains 1 water molecule per CaCO3, the amor- biogenic crystalline calcite phase. The amorphous and crystalline phous phase in the spicules is mostly anhydrous when the spicules phases are juxtaposed, often appearing in adjacent sites at a scale are extracted at an advanced developmental stage (12, 19). of tens of nanometers. We propose that the amorphous-crystal Macroscopically, therefore, the spicule displays both amorphous transformation propagates in a tortuous path through preexisting and crystalline qualities. 40- to 100-nm amorphous units, via a secondary nucleation mechanism. Results and Discussion Unraveling the mechanistic complexities of the spatial and biomineralization ͉ Ca L-edge X-ray absorption near-edge structure ͉ temporal interplay between the transforming amorphous and XANES ͉ X-PEEM ͉ X-ray photoelectron emission spectromicroscopy crystalline phases requires the use of high-resolution techniques. Here, we use X-ray photoelectron emission spectromicroscopy widespread strategy in biomineralization is the initial (X-PEEM) to study the transformation at high spatial resolution Aformation of transient amorphous precursor phases that (20, 21). We analyze X-ray absorption near-edge structure subsequently transform into one of the more stable crystalline (XANES) (22) spectra at the Ca L-edge along the length of phases (1). This process was first observed in the teeth of chitons spicules at two developmental stages. Ca spectra were acquired where a disordered ferrihydrite precursor transforms into mag- by recording 170 images, 0.1 eV apart, and arranging them in netite (2). It has also been observed in different invertebrate stacks in which the energy-dependent intensity of each pixel phyla (3–8). Amorphous calcium phosphate was recently iden- holds the full spectral information across the Ca L-edge. The tified in the newly deposited fin bones of zebrafish (9). The pixel size depends on the magnification and is 40–200 nm in this mechanistic details of these transformations are, however, still study, while the probing depth is Ϸ3nmattheCaL-edge energy poorly understood. Here, we address this fundamental issue by range (23). This technique offers the unique opportunity of studying the transformation of amorphous calcium carbonate characterizing the atomic order of the mineral phase (24) along (ACC) to crystalline calcite in the sea urchin larval spicule. Sea a single larval spicule with sub-micrometer spatial resolution, urchin larval spicules have long served as a model system for the providing time and space-resolved snapshots of the crystalliza- study of CaCO3 biomineralization processes, and the transient tion pathway through 2 distinct amorphous phases. ACC precursor phase was first identified in this system (3). The Fig. 1 shows spectra acquired from a 48-h embryo spicule with mature larval spicule is composed of a single crystal of magne- a pixel size of 200 nm. At this stage the spicule is at the triradiate sium-bearing calcite (10, 11). Small amounts of organic macro- stage of development and is composed of 70–90% ACC (18). molecules (0.1 wt%) are incorporated within the mineral and are The spectra were extracted from areas near the tip and along 1 known to play a role in the transient stabilization of the of the spicule radii. The spectra near the tip are more hetero- amorphous phase (12). geneous than those from the rest of the spicule, revealing that The spicules are formed inside a syncytium produced by newly-formed regions of the spicule are structurally diverse. specialized cells (13). The first deposit is a single rhombohedral- Similar results on a different 48-h spicule are presented in shaped calcite crystal. Further growth of the spicule radii follows supporting information (SI) Fig. S1. For comparison, spectra crystallographic orientations dictated by the initial crystal (10, 14), even though the mineral deposited is mainly in the form of Ϸ Author contributions: Y.P., I.S., L.A., and S.W. designed research; Y.P., R.A.M., M.A., F.H.W., ACC. The rays elongate rapidly for 3 days, while the existing and P.G. performed research; M.A., B.G., F.H.W., and P.G. contributed new reagents/ rays thicken. ACC is most probably introduced into the miner- analytic tools; Y.P., R.A.M., B.G., I.S., L.A., S.W., and P.G. analyzed data; and Y.P., L.A., S.W., alization site by the cells in vesicles that fuse with the syncytial and P.G. wrote the paper. membrane (15). The spicule is tightly surrounded by this mem- The authors declare no conflict of interest.
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