Mineral formation in the primary polyps of pocilloporoid corals

Maayan Neder, Pierre Philippe Laissue, Anat Akiva, Derya Akkaynak, Marie Albéric, Oliver Spaeker, Yael Politi, Iddo Pinkas, Tali Mass

Research output: Contribution to journalArticlepeer-review

Abstract

In reef-building corals, larval settlement and its rapid calcification provides a unique opportunity to study the bio-calcium carbonate formation mechanism involving skeleton morphological changes. Here we investigate the mineral formation of primary polyps, just after settlement, in two species of the pocilloporoid corals: Stylophora pistillata (Esper, 1797) and Pocillopora acuta (Lamarck, 1816). We show that the initial mineral phase is nascent Mg-Calcite, with rod-like morphology in P. acuta, and dumbbell morphology in S. pistillata. These structures constitute the first layer of the basal plate which is comparable to Rapid Accretion Deposits (Centers of Calcification, CoC) in adult coral skeleton. We found also that the rod-like/dumbbell Mg-Calcite structures in subsequent growth step will merge into larger aggregates by deposition of aragonite needles. Our results suggest that a biologically controlled mineralization of initial skeletal deposits occurs in three steps: first, vesicles filled with divalent ions are formed intracellularly. These vesicles are then transferred to the calcification site, forming nascent Mg-Calcite rod/pristine dumbbell structures. During the third step, aragonite crystals develop between these structures forming spherulite-like aggregates. Statement of Significance: Coral settlement and recruitment periods are highly sensitive to environmental conditions. Successful mineralization during these periods is vital and influences the coral's chances of survival. Therefore, understanding the exact mechanism underlying carbonate precipitation is highly important. Here, we used in vivo microscopy, spectroscopy and molecular methods to provide new insights into mineral development. We show that the primary polyp's mineral arsenal consists of two types of minerals: Mg-Calcite and aragonite. In addition, we provide new insights into the ion pathway by showing that divalent ions are concentrated in intracellular vesicles and are eventually deposited at the calcification site.

Original languageEnglish
Pages (from-to)631-645
Number of pages15
JournalActa Biomaterialia
Volume96
DOIs
StatePublished - 15 Sep 2019

Bibliographical note

Funding Information:
This work was supported by the Israel Science Foundation (Grant 312/15 ), United States-Israel Binational Science Foundation (BSF; Grant # 2016321 ), the European Research Commission (ERC; Grant # 755876 ) and the ASSEMBLE Plus consortium for an access grant (ref. SR16022018108e1) to the Inter-University Institute for Marine Sciences in Eilat.

Funding Information:
We thank Gil Goobes, Omer Yaffe, Daniel Sher and Steve Weiner for the insightful discussions and for suggesting improvements. The authors acknowledge BESSY II Synchrotron Radiation Facility for provision of synchrotron radiation facilities and the authors would like to thank the mySpot beamline scientist and local contacts Ivo Zizak and Zhaoyong Zou for assistance during beamtime. We thank Yarden Ben-Tabu De-Lion for the model illustration, Maya Lalzar and Asaf Malik from Bionformatics Core Unit, University of Haifa, Israel and the Mantoux Bioinformatics institute of the Nancy and Stephen Grand Israel National Center for Personalized Medicine, Weizmann Institute of Science, for the bioinformatics analysis. We thank Ruth Gates for supporting our research at HIMB. This work was supported by the Israel Science Foundation (Grant 312/15), United States-Israel Binational Science Foundation (BSF; Grant # 2016321), the European Research Commission (ERC; Grant # 755876) and the ASSEMBLE Plus consortium for an access grant (ref. SR16022018108e1) to the Inter-University Institute for Marine Sciences in Eilat. M.N, A.A. I.P. P.P.L, D.A, and T.M. carried out the experiments, participated in the data analysis, participated in the design of the study and drafted the manuscript; M.N. carried out the field work, SEM imaging and EDS analysis; M.N, P.P.L and T.M microscopy imaging; I.P. M.N and T.M. carried out the Raman measurement and analysis; M.N, T.M, I.P, Y.P, and M.A, carried out the XRD and XRF measurements; M.N, O.S and Y.P carried out the XRD and XRF data analysis: A.A. and T.M. carried out the cryo-SEM imaging; D.A carried out the image analysis. All authors gave their final approval for publication.

Publisher Copyright:
© 2019 Acta Materialia Inc.

Keywords

  • Aragonite
  • Dumbbell
  • Mg-Calcite
  • Spherulitic growth
  • Vesicles

ASJC Scopus subject areas

  • Biotechnology
  • Biomaterials
  • Biochemistry
  • Biomedical Engineering
  • Molecular Biology

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