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A Modern Scleractinian Coral with a Two-Component Calcite–Aragonite Skeleton

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A Modern Scleractinian Coral with a Two-Component Calcite–Aragonite Skeleton A modern scleractinian coral with a two-component calcite–aragonite skeleton Jarosław Stolarskia,1, Ismael Coronadob, Jack G. Murphyc, Marcelo V. Kitaharad,e, Katarzyna Janiszewskaa, Maciej Mazurf, Anne M. Gothmanng,h, Anne-Sophie Bouvieri, Johanna Marin-Carbonnei, Michelle L. Taylorj, Andrea M. Quattrinik,l, Catherine S. McFaddenl, John A. Higginsc, Laura F. Robinsonm, and Anders Meibomi,n aInstitute of Paleobiology, Polish Academy of Sciences, PL-00-818 Warsaw, Poland; bFaculty of Biological and Environmental Sciences, University of Leon, 24171 Leon, Spain; cDepartment of Geosciences, Princeton University, Princeton, NJ 08544; dMarine Science Department, Federal University of São Paulo, 11070-100 Santos (SP), Brazil; eCentre for Marine Biology, University of São Paulo, 11612-109 São Sebastião (SP), Brazil; fDepartment of Chemistry, University of Warsaw, PL-02-093 Warsaw, Poland; gDepartment of Environmental Studies, St. Olaf College, Northfield, MN 55057; hDepartment of Physics, St. Olaf College, Northfield, MN 55057; iCenter for Advanced Surface Analysis, Institute of Earth Sciences, Université de Lausanne, CH-1015 Lausanne, Switzerland; jSchool of Life Sciences, University of Essex, Wivenhoe Park, CO4 3SQ Colchester, United Kingdom; kDepartment of Invertebrate Zoology, Smithsonian Institution, Washington, DC 20560-0163; lDepartment of Biology, Harvey Mudd College, Claremont, CA 91711; mSchool of Earth Sciences, University of Bristol, BS8 1RJ Clifton, United Kingdom; and nLaboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland Edited by Paul G. Falkowski, Rutgers University, New Brunswick, NJ, and approved November 4, 2020 (received for review June 29, 2020) One of the most conserved traits in the evolution of biomineraliz- high-Mg calcite (HMC) precipitation at Mg/Ca > 2 mol/mol ing organisms is the taxon-specific selection of skeletal minerals. (“aragonitic seas”) (5, 6). During the mid-Cretaceous, the Mg/Ca All modern scleractinian corals are thought to produce skeletons ratio is thought to have been well below 2 mol/mol (7, 8), creating exclusively of the calcium-carbonate polymorph aragonite. De- conditions conducive to calcite precipitation. Despite that, only one spite strong fluctuations in ocean chemistry (notably the Mg/Ca scleractinian coral, Coelosmilia from Upper Cretaceous chalk de- ratio), this feature is believed to be conserved throughout the posits, has, to date, been documented to have a bona fide primary coral fossil record, spanning more than 240 million years. Only calcitic skeleton (9). This observation is consistent with biomineralizing one example, the Cretaceous scleractinian coral Coelosmilia (ca. organisms exerting stronger control over polymorph selection than a 70 to 65 Ma), is thought to have produced a calcitic skeleton. Here, simple inorganic precipitation process. we report that the modern asymbiotic scleractinian coral Paraco- Coral skeletal microstructural patterns are highly conserved EVOLUTION notrochus antarcticus living in the Southern Ocean forms a two- through evolution and have often been used to elucidate phy- component carbonate skeleton, with an inner structure made of logenetic relationships in the absence of genetic information high-Mg calcite and an outer structure composed of aragonite. P. (10). Corals exhibiting similar microstructure very likely share a antarcticus and Cretaceous Coelosmilia skeletons share a unique similar origin. Indeed, the biomineralization process has proven microstructure indicating a close phylogenetic relationship, consis- to be robust enough to withstand dramatic environmental changes tent with the early divergence of P. antarcticus within the Vacatina throughout geological time, including substantial changes in sea- (i.e., Robusta) clade, estimated to have occurred in the Mesozoic water chemistry (11, 12). (ca. 116 Mya). Scleractinian corals thus join the group of marine In this context, we report the discovery that the extant, deep- EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES organisms capable of forming bimineralic structures, which re- sea, solitary, scleractinian coral Paraconotrochus antarcticus, quires a highly controlled biomineralization mechanism; this capa- which is ubiquitous in the Southern Ocean around Antarctica bility dates back at least 100 My. Due to its relatively prolonged isolation, the Southern Ocean stands out as a repository for extant Significance marine organisms with ancient traits. Until now, all of the ca. 1,800 known modern scleractinian coral biomineralization | calcium carbonate | scleractinian corals | evolution | species were thought to produce skeletons exclusively of ara- Southern Ocean gonite. Asymbiotic Paraconotrochus antarcticus living in the Southern Ocean is the first example of an extant scleractinian he ability to form a calcium carbonate skeleton represents an that forms a two-component carbonate skeleton, with an inner Tevolutionary innovation of major importance that dates back structure made of high-Mg calcite and an outer structure to the onset of the Phanerozoic (ca. 540 Ma) (1). Since that time, composed of aragonite. This discovery adds support to the multiple groups of marine metazoans became highly efficient notion that the coral skeletal formation process is strongly bi- reef builders, creating the structural foundation for the richest ologically controlled. Mitophylogenomic analysis shows that P. and most biodiverse ecosystems in the ocean (2). In our modern antarcticus represents an ancient scleractinian clade, suggest- ocean, carbonate reef building is dominated by scleractinian ing that skeletal mineralogy/polymorph of a taxon, once corals, which produce ∼1012 kg of skeleton carbonate every year established, is a trait conserved throughout the evolution of (3). Based on available empirical evidence, it is widely accepted that clade. that pristine skeletons of modern scleractinians, grown in natural environments, consist exclusively of the carbonate polymorph Author contributions: J.S. designed research; J.S., I.C., J.G.M., M.V.K., K.J., M.M., A.-S.B., and J.M.-C. performed research; J.S., I.C., J.G.M., M.V.K., K.J., M.M., A.M.G., A.-S.B., J.M.-C., aragonite, which is metastable at ambient conditions typical of M.L.T., A.M.Q., C.S.M., J.A.H., L.F.R., and A.M. analyzed data; and J.S., I.C., J.G.M., M.V.K., and the Earth’s surface. A.M. wrote the paper. In vitro experiments under ambient temperatures show that The authors declare no competing interest. abiotic precipitation of calcium carbonate polymorphs from This article is a PNAS Direct Submission. seawater is controlled primarily by the Mg/Ca ratio (4). With This open access article is distributed under Creative Commons Attribution-NonCommercial- present-day ionic strengths and atmospheric CO2 concentration NoDerivatives License 4.0 (CC BY-NC-ND). (pH ca. 8), the seawater Mg/Ca ratio (today 5.2 mol/mol) sepa- 1To whom correspondence may be addressed. Email: [email protected]. rates two regimes of inorganic carbonate polymorph precipita- This article contains supporting information online at https://www.pnas.org/lookup/suppl/ tion: the regime of low-magnesium calcite (LMC) at Mg/Ca < doi:10.1073/pnas.2013316117/-/DCSupplemental. 2 mol/mol (“calcitic seas”) and the regime of aragonite and/or Published December 15, 2020. PNAS 2021 Vol. 118 No. 3 e2013316117 https://doi.org/10.1073/pnas.2013316117 | 1of8 Downloaded by guest on September 27, 2021 (13) at depths between 50 and 700 m and at temperatures be- and aragonitic regions (Fig. 2 L and M). The calcitic inner tween ca. 0.5 and 3 °C, forms a two-component calcite–aragonite skeleton is depleted in Sr and Na and enriched in Mg, averaging skeleton with microstructural features very similar to the Cre- ca. 11 mole percent (mol%) of MgCO3 and thus compositionally taceous Coelosmilia (Fig. 1 and SI Appendix, Fig. S1). HMC, which is consistent with the observed Raman peak shifts relative to the LMC (Fig. 2I). The aragonitic outer skeleton Results contains ca. 1.2 mol% SrCO3, with MgCO3 below the electron The samples of P. antarcticus studied here include both bare microprobe detection limit, that is, similar to aragonitic skele- skeletons and specimens collected alive, obtained from material tons of other deep-sea corals (15). dredged from the Weddell, Ross, and Cooperation seas, re- Both aragonitic and calcitic crystals have the a and b axis ro- spectively (SI Appendix, Fig. S2 and Table S1). The skeleton of P. tated around the c axis (turbostratic distribution) in the plane antarcticus is shaped like a regular cone, which is a few centi- (222) of aragonite and (1014) of calcite (Fig. 2 F–H). Raman A B SI Ap- meters in both diameter and height (Fig. 1 and and spectra in RADs and neighboring TD regions indicated disor- pendix A B , Fig. S1 and ). Its septa are hexamerally arranged in dered material in both calcite and aragonite RADs (Fig. 2 I–K). five cycles, and the central portion of the calice is occupied by The aragonitic RADs showed stronger fluorescence than RADs labyrinthine projections (so-called columella). in the calcitic inner skeleton (SI Appendix, Fig. S9 A and B). n = P antarcticus In transversal cuts ( 31), all examined . con- The measured average 44Ca/40Ca isotope ratios of the arago- sistently revealed a distinct boundary between two main skeletal nitic and calcitic skeletal parts were −1.51 ± 0.21‰ and −1.24 ± regions, hereafter referred to as the inner and outer skeleton ‰ σ δ44/40 E F H–J 0.14 (relative to seawater, 2 ). The mean Ca value of the (Fig. 1 , , and ). The inner skeleton is relatively narrow inner calcitic skeleton is consistent with that observed in other (ca. 50 to 100 μm thick) and forms the central parts of the septa E H–J biomineralizers that form HMC and have sophisticated control and wall (Fig. 1 and ). This inner skeleton is also observ- over biomineralization. The average δ44/40Ca value of the ara- able at the distalmost (upper) growth front of the calice, where it gonitic outer skeleton is consistent with other biogenic arago- is deposited quasi-contemporaneously with the outer skeleton C D nites.
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