Growth and regrowth of adult sea urchin spines involve hydrated and anhydrous amorphous calcium carbonate precursors

Albéric, Marie; Stifler, Cayla A.; Zou, Zhaoyong; Sun, Chang‐Yu; Killian, Christopher E.; València, S.; Mawass, Mohamad‐Assaad; Bertinetti, Luca; Gilbert, Benjamin; Politi, Yael

doi:10.1016/j.yjsbx.2019.100004

Cited by 22 publications

(33 citation statements)

References 58 publications

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“…The new CY1 components ACC-H 2 O, ACC, and aragonite are presented in SI Appendix, Fig. S1 and are consistent with all previously published spectra ( 33 , 36 – 39 , 75 ).…”

Section: Methodssupporting

confidence: 89%

From particle attachment to space-filling coral skeletons

Sun

Stifler

Chopdekar

et al. 2020

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

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Reef-building corals and their aragonite (CaCO3) skeletons support entire reef ecosystems, yet their formation mechanism is poorly understood. Here we used synchrotron spectromicroscopy to observe the nanoscale mineralogy of fresh, forming skeletons from six species spanning all reef-forming coral morphologies: Branching, encrusting, massive, and table. In all species, hydrated and anhydrous amorphous calcium carbonate nanoparticles were precursors for skeletal growth, as previously observed in a single species. The amorphous precursors here were observed in tissue, between tissue and skeleton, and at growth fronts of the skeleton, within a low-density nano- or microporous layer varying in thickness from 7 to 20 µm. Brunauer-Emmett-Teller measurements, however, indicated that the mature skeletons at the microscale were space-filling, comparable to single crystals of geologic aragonite. Nanoparticles alone can never fill space completely, thus ion-by-ion filling must be invoked to fill interstitial pores. Such ion-by-ion diffusion and attachment may occur from the supersaturated calcifying fluid known to exist in corals, or from a dense liquid precursor, observed in synthetic systems but never in biogenic ones. Concomitant particle attachment and ion-by-ion filling was previously observed in synthetic calcite rhombohedra, but never in aragonite pseudohexagonal prisms, synthetic or biogenic, as observed here. Models for biomineral growth, isotope incorporation, and coral skeletons’ resilience to ocean warming and acidification must take into account the dual formation mechanism, including particle attachment and ion-by-ion space filling.

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“…The new CY1 components ACC-H 2 O, ACC, and aragonite are presented in SI Appendix, Fig. S1 and are consistent with all previously published spectra ( 33 , 36 – 39 , 75 ).…”

Section: Methodssupporting

confidence: 89%

From particle attachment to space-filling coral skeletons

Sun

Stifler

Chopdekar

et al. 2020

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

Self Cite

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“…Generally, it has been suggested that the denser structure of partially or fully dehydrated ACC might display some resemblance to one of the anhydrous crystalline CaCO 3 polymorphs . More recently, the short‐range order of ACC particles possessing different degrees of hydration was qualitatively characterized with O K‐edge and Ca L‐edge XANES techniques that are more sensitive towards structural changes. The features of anhydrous ACC are distinctly different from those of hydrated ACC with n= 1.…”

Section: Structure and Hydration Of Accmentioning

confidence: 99%

Water: How Does It Influence the CaCO₃ Formation?

Amstad

2019

Angew Chem Int Ed

124

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Nature produces biomineral‐based materials with a fascinating set of properties using only a limited number of elements. This set of properties is obtained by closely controlling the structure and local composition of the biominerals. We are far from achieving the same degree of control over the properties of synthetic biomineral‐based composites. One reason for this inferior control is our incomplete understanding of the influence of the synthesis conditions and additives on the structure and composition of the forming biominerals. In this Review, we provide an overview of the current understanding of the influence of synthesis conditions and additives during different formation stages of CaCO3, one of the most abundant biominerals, on the structure, composition, and properties of the resulting CaCO3 crystals. In addition, we summarize currently known means to tune these parameters. Throughout the Review, we put special emphasis on the role of water in mediating the formation of CaCO3 and thereby influencing its structure and properties, an often overlooked aspect that is of high relevance.

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“…The Mg‐calcite skeleton of echinoderms consists of numerous ossicles with a distinct tridimensional porous microstructure termed stereom that is formed through the initial deposition of amorphous calcium carbonate (ACC) with different hydration levels (e.g., Alberic et al, 2019). Despite a highly controlled intracellular biomineralization process, environmental controls on the elemental composition of the echinoderm skeleton have been evidenced.…”

Section: Introductionmentioning

confidence: 99%

Effects of seawater Mg²⁺/Ca²⁺ ratio and diet on the biomineralization and growth of sea urchins and the relevance of fossil echinoderms to paleoenvironmental reconstructions

et al. 2020

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It has been argued that skeletal Mg/Ca ratio in echinoderms is mostly governed by Mg 2+ and Ca 2+ concentrations in the ambient seawater. Accordingly, well-preserved fossil echinoderms were used to reconstruct Phanerozoic seawater Mg 2+ /Ca 2+ ratio. However, Mg/Ca ratio in echinoderm skeleton can be affected by a number of environmental and physiological factors, the effects of which are still poorly understood. Notably, experimental data supporting the applicability of echinoderms in paleoenvironmental reconstructions remain limited. Here, we investigated the effect of ambient Mg 2+ /Ca 2+ seawater ratio and diet on skeletal Mg/Ca ratio and growth rate in two echinoid species (Psammechinus miliaris and Prionocidaris baculosa). Sea urchins were tagged with manganese and then cultured in different Mg 2+ /Ca 2+ conditions to simulate fluctuations in the Mg 2+ /Ca 2+ seawater ratios in the Phanerozoic. Simultaneously, they were fed on a diet containing different amounts of magnesium. Our results show that the skeletal Mg/Ca ratio in both species varied not only between ossicle types but also between different types of stereom within a single ossicle. Importantly, the skeletal Mg/Ca ratio in both species decreased proportionally with decreasing seawater Mg 2+ /Ca 2+ ratio. However, sea urchins feeding on Mg-enriched diet produced a skeleton with a higher Mg/Ca ratio. We also found that although incubation in lower ambient Mg 2+ /Ca 2+ ratio did not affect echinoid respiration rates, it led to a decrease or inhibition of their growth. Overall, these results demonstrate that although skeletal Mg/Ca ratios in echinoderms can be largely determined by seawater chemistry, the type of diet may also influence skeletal geochemistry, which imposes constraints on the application of fossil echinoderms as a reliable proxy. The accuracy of paleoseawater Mg 2+ /Ca 2+ calculations is further limited by the fact that Mg partition coefficients vary significantly at different scales (between species, specimens feeding on different types of food, different ossicle types, and stereom types within a single ossicle).

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Growth and regrowth of adult sea urchin spines involve hydrated and anhydrous amorphous calcium carbonate precursors

Cited by 22 publications

References 58 publications

From particle attachment to space-filling coral skeletons

From particle attachment to space-filling coral skeletons

Water: How Does It Influence the CaCO₃ Formation?

Effects of seawater Mg²⁺/Ca²⁺ ratio and diet on the biomineralization and growth of sea urchins and the relevance of fossil echinoderms to paleoenvironmental reconstructions

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Growth and regrowth of adult sea urchin spines involve hydrated and anhydrous amorphous calcium carbonate precursors

Cited by 22 publications

References 58 publications

From particle attachment to space-filling coral skeletons

From particle attachment to space-filling coral skeletons

Water: How Does It Influence the CaCO3 Formation?

Effects of seawater Mg2+/Ca2+ ratio and diet on the biomineralization and growth of sea urchins and the relevance of fossil echinoderms to paleoenvironmental reconstructions

Contact Info

Product

Resources

About

Water: How Does It Influence the CaCO₃ Formation?

Effects of seawater Mg²⁺/Ca²⁺ ratio and diet on the biomineralization and growth of sea urchins and the relevance of fossil echinoderms to paleoenvironmental reconstructions