Acid polysaccharides in the skeletal matrix and calicoblastic epithelium of the stony coral Mycetophyllia reesi

Goldberg, W. M.

doi:10.1054/tice.2001.0191

Cited by 60 publications

(36 citation statements)

References 36 publications

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“…The calcification rates in M. digitata cell cultures were approximately an order of magnitude higher than those in X. elongata Skeletal Organic Matrix. Studies of coral biomineralization indicate that calcification is mediated by the synthesis of an organic framework that induces nucleation and crystal growth (4,5,36,37). Analyses of the organic materials extracted from coral skeletons show a composition of acidic amino acids (mainly glutamic and aspartic acid) and sulfated polysaccharides (5,(38)(39)(40)(41).…”

Section: Resultsmentioning

confidence: 99%

Extracellular matrix production and calcium carbonate precipitation by coral cells in vitro

Helman¹,

Natale²,

Sherrell

et al. 2008

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

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The evolution of multicellularity in animals required the production of extracellular matrices that serve to spatially organize cells according to function. In corals, three matrices are involved in spatial organization: (i) an organic ECM, which facilitates cell-cell and cell-substrate adhesion; (ii) a skeletal organic matrix (SOM), which facilitates controlled deposition of a calcium carbonate skeleton; and (iii) the calcium carbonate skeleton itself, which provides the structural support for the 3D organization of coral colonies. In this report, we examine the production of these three matrices by using an in vitro culturing system for coral cells. In this system, which significantly facilitates studies of coral cell physiology, we demonstrate in vitro excretion of ECM by primary (nondividing) tissue cultures of both soft (Xenia elongata) and hard (Montipora digitata) corals. There are structural differences between the ECM produced by X. elongata cell cultures and that of M. digitata, and ascorbic acid, a critical cofactor for proline hydroxylation, significantly increased the production of collagen in the ECM of the latter species. We further demonstrate in vitro production of SOM and extracellular mineralized particles in cell cultures of M. digitata. Inductively coupled plasma mass spectrometry analysis of Sr/Ca ratios revealed the particles to be aragonite. De novo calcification was confirmed by following the incorporation of 45 Ca into acid labile macromolecules. Our results demonstrate the ability of isolated, differentiated coral cells to undergo fundamental processes required for multicellular organization.aragonite ͉ cell culture ͉ cnidaria ͉ calcification ͉ C orals (class, Anthozoa) are the most basal cnidarians and the first animal phylum with an organized neural system and complex active behavior (1). The embryonic gastrula develops to form an outer ectoderm and an inner endoderm separated by the mesoglea, a noncellular fibrous jelly-like material (2). The two germ layers are spatially structured by an ECM in which embedded, interstitial (stem) cells give rise to nematocysts, mucous glands, and sensory or nerve cells (2, 3). Many corals also precipitate calcium carbonate in the form of aragonite on a skeletal organic matrix (SOM) template (4, 5). The precipitation pattern is highly controlled between colonies, giving rise to morphological structures that are used as primary phenotypic markers of species in extant reefs and fossil samples.The basic cellular processes responsible for the production of ECM, SOM, and calcium carbonate skeleton remain largely unknown. Molecular, genetic, and physiological analyses of cellular processes in corals have been elusive mainly because it is difficult to grow corals under controlled conditions in the laboratory and because of the genetic and physiological complexities inherent in associations of the animals with symbionts and parasites. All zooxanthellate corals harbor intracellular symbiotic dinoflagellates (zooxanthellae) within their endoderm cells; the al...

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Section: Resultsmentioning

confidence: 99%

Extracellular matrix production and calcium carbonate precipitation by coral cells in vitro

Helman¹,

Natale²,

Sherrell

et al. 2008

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

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“…First, organic matter coats aragonite crystals in the skeleton (Clode and Marshall, 2002), and elevated organic matter content is closely associated with the relatively disordered centers of calcification (COCs; also called "rapid accretion deposits" or RADs) (Benzerara et al, 2011;Falini et al, 2013;Von Euw et al, 2017). Second, organic molecules extracted from the skeleton have been attributed to certain roles in crystal growth (Constantz and Weiner, 1988;Weiner and Addadi, 1991;Allemand et al, 1998;Goldberg, 2001;Cuif et al, 2008;Reggi et al, 2014;Takeuchi et al, 2016), with some proteins even capable of inducing spontaneous aragonite precipitation from seawater . Finally, the unit cell of biogenic aragonite contracts after annealing (i.e., heating and allowing to cool), presumably due to the removal of the SOM from the lattice (Pokroy et al, 2004;Reggi et al, 2014;Zolotoyabko, 2017).…”

Section: Introductionmentioning

confidence: 99%

The Origin and Role of Organic Matrix in Coral Calcification: Insights From Comparing Coral Skeleton and Abiogenic Aragonite

DeCarlo¹,

Ren²,

Farfán³

2018

Front. Mar. Sci.

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Understanding the mechanisms of coral calcification is critical for accurately projecting coral reef futures under ocean acidification and warming. Recent suggestions that calcification is primarily controlled by organic molecules and the biological activity of the coral polyp imply that ocean acidification may not affect skeletal accretion. The basis for these suggestions relies heavily on correlating the presence of organic matter with the orientation and disorder of aragonite crystals in the skeleton, carrying the assumption that organic matter observed in the skeleton was produced by the polyp to control calcification. Here we use Raman spectroscopy to test whether there are differences in organic matter content between coral skeleton and abiogenic aragonites precipitated from seawater, both before and after thermal annealing (heating). We measured the background fluorescence and intensity of C-H bonding signals in the Raman spectra, which are commonly attributed to coral polyp-derived skeletal organic matrix (SOM) and have been used to map its distribution. Surprisingly, we found no differences in either fluorescence or C-H bonding between abiogenic aragonite and coral skeleton. Annealing reduced the molecular disorder in coral skeleton, potentially due to removal of organic matter, but the same effect was also observed in the abiogenic aragonites. The presence of organic molecules in the abiogenic aragonites is further supported by measurements of N content and δ 15 N. Together, our data suggest that some of what has been interpreted in previous studies as polyp-derived SOM may actually be seawater-sourced organic matter or some other signal not unique to biogenic aragonite. Finally, we create a high-resolution Raman map of a Pocillopora skeleton to demonstrate how patterns of fluorescence and elevated calcifying fluid aragonite saturation state ( Ar ) along centers of calcification are consistent with both biological and physico-chemical controls. Our aim is to advance discussion on biological mediation of calcification and the implications for coral resilience in a high-CO 2 world.

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“…In corals, the production of organic material is thought to be a prerequisite for calcification (23), with protein synthesis closely associated with calicodermal cells (24)(25)(26). The first published proteome analysis of the SOM in a stony coral (27) revealed a group of coral acid-rich proteins (CARPs) that can spontaneously catalyze the precipitation of calcium carbonate in vitro (28).…”

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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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Acid polysaccharides in the skeletal matrix and calicoblastic epithelium of the stony coral Mycetophyllia reesi

Cited by 60 publications

References 36 publications

Extracellular matrix production and calcium carbonate precipitation by coral cells in vitro

Extracellular matrix production and calcium carbonate precipitation by coral cells in vitro

The Origin and Role of Organic Matrix in Coral Calcification: Insights From Comparing Coral Skeleton and Abiogenic Aragonite

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

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