XANES mapping of organic sulfate in three scleractinian coral skeletons

Cuif, Jean‐Pierre; Dauphin, Yannicke; Doucet, J.; Salomé, Murielle; Susini, J.

doi:10.1016/s0016-7037(02)01041-4

Cited by 224 publications

(231 citation statements)

References 11 publications

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“…This article is a PNAS Direct Submission. 1 To whom correspondence should be sent at the present address: Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany. E-mail: lnooijer@awi.de.…”

Section: Resultsmentioning

confidence: 99%

Foraminifera promote calcification by elevating their intracellular pH

Nooijer

Toyofuku²,

Kitazato³

2009

Proc. Natl. Acad. Sci. U.S.A.

293

262

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Surface seawaters are supersaturated with respect to calcite, but high concentrations of magnesium prevent spontaneous nucleation and growth of crystals. Foraminifera are the most widespread group of calcifying organisms and generally produce calcite with a low Mg content, indicating that they actively remove Mg 2؉ from vacuolized seawater before calcite precipitation. However, one order of foraminifera has evolved a calcification pathway, by which it produces calcite with a very high Mg content, suggesting that these species do not alter the Mg/Ca ratio of vacuolized seawater considerably. The cellular mechanism that makes it possible to precipitate calcite at high Mg concentrations, however, has remained unknown. Here we demonstrate that they are able to elevate the pH at the site of calcification by at least one unit above seawater pH and, thereby, overcome precipitation-inhibition at ambient Mg concentrations. A similar result was obtained for species that precipitate calcite with a low Mg concentration, suggesting that elevating the pH at the site of calcification is a widespread strategy among foraminifera to promote calcite precipitation. Since the common ancestor of these two groups dates back to the Cambrian, our results would imply that this physiological mechanism has evolved over half a billion years ago. Since foraminifera rely on elevating the intracellular pH for their calcification, our results show that ongoing ocean acidification can result in a decrease of calcite production by these abundant calcifyers.benthic foraminifera ͉ foraminiferal evolution ͉ ocean acidification A large variety of organisms that form skeletons of calciumcarbonate have evolved over the last half billion years. Some groups precipitate predominantly aragonite, such as scleractinian corals (1) and calcareous chlorophytes (2), others mostly calcite, such as foraminifera (3), coccolithophores (4), and corraline Rhodophytes (2), and some a chimera of the two (5,6). The geological prevalence of the different groups is thought to be caused by successions in sea water chemistry: periods with relatively high Ca 2ϩ concentrations and low Mg 2ϩ concentrations (i.e., with low Mg/Ca ratios) have favored organisms precipitating calcite, while periods with relatively high Mg/Ca ratios (e.g., during the Neogene) have favored those forming aragonite (7-9). For foraminifera, the relation between ocean chemistry and their evolution is less clear (10) and possibly obscured by the existence of different calcification strategies in this group.Calcifying foraminifera are commonly divided into two groups according to their test (i.e., shell) structure: miliolid and hyaline. Miliolids precipitate calcite in the form of needles with a length of 2-3 m within cytoplasmic vesicles (11, 12) (see: 13 for the only known exception in this taxon). Before chamber formation, these needles accumulate in the cell and form a new chamber after simultaneous transport outside the test and assembly within an organic matrix (14). The needles forming the outer lay...

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Section: Resultsmentioning

confidence: 99%

Foraminifera promote calcification by elevating their intracellular pH

Nooijer

Toyofuku²,

Kitazato³

2009

Proc. Natl. Acad. Sci. U.S.A.

293

262

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“…However, a recent study using secondary ion mass spectrometry shows that the two common microstructural components, centers of calcification and fibers, are produced during day and night (59). In addition, in asymbiotic deep-sea corals, EMZs and fibrous layers have been observed (21). Regardless of the timing, however, at each growth step, the secreted organic matrices remain entrapped within the crystalline units whose growth they control, leading to the formation of heterologous structures revealed by the etching process (16).…”

Section: Discussionmentioning

confidence: 99%

“…X-ray absorption near edge structure spectroscopy mapping, at the micrometer scale, has established that the SOM is associated with the mineral phase within each growth layer (21). Recently, it was suggested that each couplet of organic-seed (e.g., negative etching) and fiber interaction represents a single 24-h period (22).…”

mentioning

confidence: 99%

Immunolocalization of skeletal matrix proteins in tissue and mineral of the coralStylophora pistillata

Mass

Drake

Peters

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

104

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The precipitation and assembly of calcium carbonate skeletons by stony corals is a precisely controlled process regulated by the secretion of an ECM. Recently, it has been reported that the proteome of the skeletal organic matrix (SOM) contains a group of coral acid-rich proteins as well as an assemblage of adhesion and structural proteins, which together, create a framework for the precipitation of aragonite. To date, we are aware of no report that has investigated the localization of individual SOM proteins in the skeleton. In particular, no data are available on the ultrastructural mapping of these proteins in the calcification site or the skeleton. This information is crucial to assessing the role of these proteins in biomineralization. Immunological techniques represent a valuable approach to localize a single component within a calcified skeleton. By using immunogold labeling and immunohistochemical assays, here we show the spatial arrangement of key matrix proteins in tissue and skeleton of the common zooxanthellate coral, Stylophora pistillata. To our knowledge, our results reveal for the first time that, at the nanoscale, skeletal proteins are embedded within the aragonite crystals in a highly ordered arrangement consistent with a diel calcification pattern. In the tissue, these proteins are not restricted to the calcifying epithelium, suggesting that they also play other roles in the coral's metabolic pathways.actin | carbonic anhydrase | CARPs | cadherins C orals (phylum Cnidaria) belong to one of the oldest invertebrate phyla and are one of the earliest metazoans to possess an organized body structure (reviewed in ref.

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“…15 The change in crystal domain sizes and orientations as trabeculae develop may be associated with passive or active biological control on the growth environment such as pH 11 or the presence of organic molecules. 55 Previous studies showed that by precisely controlling high supersaturation states, thus high driving forces and high growth rates, along with controlled temperature, it is possible to obtain abiotic spherulitic growth with different polymorphs of CaCO 3 . 79,81 However, whether these spherulites result from classical ion-by-ion crystal growth from solution or from other crystal growth modes has never been demonstrated.…”

mentioning

confidence: 99%

Spherulitic Growth of Coral Skeletons and Synthetic Aragonite: Nature’s Three-Dimensional Printing

Sun¹,

Marcus

Frazier³

et al. 2017

ACS Nano

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Coral skeletons were long assumed to have a spherulitic structure, that is, a radial distribution of acicular aragonite (CaCO 3 ) crystals with their c-axes radiating from series of points, termed centers of calcification (CoCs). This assumption was based on morphology alone, not on crystallography. Here we measure the orientation of crystals and nanocrystals and confirm that corals grow their skeletons in bundles of aragonite crystals, with their caxes and long axes oriented radially and at an angle from the CoCs, thus precisely as expected for feather-like or "plumose" spherulites. Furthermore, we find that in both synthetic and coral aragonite spherulites at the nanoscale adjacent crystals have similar but not identical orientations, thus demonstrating by direct observation that even at nanoscale the mechanism of spherulite formation is non-crystallographic branching (NCB), as predicted by theory. Finally, synthetic aragonite spherulites and coral skeletons have similar angle spreads, and angular distances of adjacent crystals, further confirming that coral skeletons are spherulites. This is important because aragonite grows anisotropically, 10 times faster along the c-axis than along the a-axis direction, and spherulites fill space with crystals growing almost exclusively along the c-axis, thus they can fill space faster than any other aragonite growth geometry, and create isotropic materials from anisotropic crystals. Greater space filling rate and isotropic mechanical behavior are key to the skeleton's supporting function and therefore to its evolutionary success. In this sense, spherulitic growth is Nature's 3D printing. KEYWORDS: Ion attachment, crystallization by particle attachment, CPA, biomineralization, PEEM, PIC-mapping, mesocrystal S pherulites are polycrystalline structures in which acicular crystals radiate from a common center and grow approximately synchronously so the final shape of a spherulite resembles a sphere. 1−7 Figure 1 shows two types of spherulites: "spherical spherulite", in which the crystal fibers start from a point, or "plumose spherulite", in which crystal fibers radiate at an angle from the line. 7 Spherulites start forming as an aggregate of parallel acicular crystals termed "fibers", then form a "sheaf of wheat" structure, and with the growth of more fibers eventually become complete spheres. 8 In an ideal spherulite, fibers radiate from the center and contain all possible orientations within the sphere. Since the fast-growing axis in aragonite (CaCO 3 ) is the c-axis, 9 in spherulites each fiber elongation direction coincides with the crystalline c-axis. 10,11 In real spherulites, biogenic 12 and synthetic, 7 the crystal orientations are not perfectly radial nor continuously varying with angle, they deviate slightly from radial and exhibit small but abrupt changes in orientation, termed "branching". In Figure 1 branching angles are smaller than 30°in direction and in crystal lattice orientation. This is distinct from crystallographic branching, which occurs in sno...

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XANES mapping of organic sulfate in three scleractinian coral skeletons

Cited by 224 publications

References 11 publications

Foraminifera promote calcification by elevating their intracellular pH

Foraminifera promote calcification by elevating their intracellular pH

Immunolocalization of skeletal matrix proteins in tissue and mineral of the coralStylophora pistillata

Spherulitic Growth of Coral Skeletons and Synthetic Aragonite: Nature’s Three-Dimensional Printing

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