pubs.acs.org/cm Published on Web 12/02/2009 r 2009 American Chemical Society Chem. Mater. 2010, 22, 161–166 161 DOI:10.1021/cm902674h Role of Magnesium Ion in the Stabilization of Biogenic Amorphous Calcium Carbonate: A Structure-Function Investigation Yael Politi, † David R. Batchelor, ‡ Paul Zaslansky, § Bradley F. Chmelka, ^ James C. Weaver, ) Irit Sagi, † Steve Weiner, † and Lia Addadi* ,† † Department of Structural Biology, Weizmann Institute of Science, Rehovot 76100, Israel, ‡ Forschungszentrum Karlsruhe GmbH, Institut f € ur Synchrotronstrahlung, D-76344 Germany, § Department of Biomaterials, Max-Planck Institute of Colloids and Interfaces, Potsdam D-14424 Germany, ^ Department of Chemical Engineering, University of California, Santa Barbara, California 93106, and ) Department of Chemical and Environmental Engineering, University of California, Riverside, California 92521 Received August 30, 2009. Revised Manuscript Received October 20, 2009 Magnesium is a key component used by many organisms in biomineralization. One role for magnesium is in stabilizing an otherwise unstable amorphous calcium carbonate (ACC) phase. The way in which this stabilization is achieved is unknown. Here, we address this question by studying the chemical environment around magnesium in biogenic and synthetic ACCs using Mg K-edge X-ray absorption spectroscopy (XAS). We show that although the short-range structure around the Mg ion is different in the various minerals studied, they all involve a shortening of the Mg-O bond length compared to crystalline anhydrous MgCO 3 minerals. We propose that the compact structure around magnesium introduces distortion in the CaCO 3 host mineral, thus inhibiting its crystallization. This study also shows that despite technical challenges in the soft X-ray energy regime, Mg K-edge XAS is a valuable tool for structural analysis of Mg containing amorphous materials, in biology and materials science. Introduction Magnesium is an essential ion in biology, used by all living organisms in many metabolic cycles, including respiration and photosynthesis. In today’s seawater, Mg is approximately five times more abundant than Ca. 1 Despite this, of the 65 or so known biogenic minerals listed by Lowenstam and Weiner, 2 only five have Mg as a major component, and none of these is widely distributed among different organisms. Mg is, however, common as an additive in carbonate and phosphate biogenic minerals. Specifically, in calcite, the Mg concentrations can vary from essentially zero to up to 30 mol % 3 and in one exceptional case, above 40 mol %. 4 Moreover, the Mg concentrations can also vary in different areas within a single crystalline skeletal element. 5 Clearly, the amount of Mg in these minerals is carefully regulated. Magnesium is surprisingly common in pathologically deposited minerals 6 and also contributes to the mechanical proper- ties of biologically produced calcites. In the sea urchin tooth, the higher Mg concentrations in the central work- ing part of the tooth are thought to be responsible for the increased hardness of this region 7 and thus indirectly contribute to the self-sharpening characteristics of the tooth. 5 These observations raise the intriguing possibility that Mg plays an important direct and indirect role in biogenic mineral formation. In vitro, Mg has a large effect on calcium carbonate precipitation. In saturated solutions with a Mg/Ca ratio of up to 2:1, Mg is incorporated in low concentrations (1-3 mol %) into calcite in the Ca lattice positions. Concomitantly, the calcite morphology is altered 8 and the unit cell parameters decrease because of the size difference between Ca and Mg ions. 9 At a Mg/Ca ratio >4 in the precipitating solution, calcite nucleation is inhibited and aragonite or amorphous calcium carbonate (ACC) precipitate instead. 10-12 The kinetic inhibition of calcite crystallization is thought to be related to the higher *Corresponding author. E-mail: Lia.Addadi@weizmann.ac.il. Tel: þ972 89342228. Fax: þ972 89344136. (1) Lippmann, F. Sedimentary Carbonate Minerals; Springer Verlag: Berlin, 1973. (2) Lowenstam, H. A.; Weiner, S. On Biomineralization; Oxford Uni- versity Press: New York, 1989; p 324. (3) Chave, K. E. J. Geol. 1954, 62, 266–283. (4) Ma, Y.; Aichmayer, B.; Paris, O.; Fratzl, P.; Meibom, A.; Metzler, R. A.; Politi, Y.; Addadi, L.; Gilbert, P. U. P. A.; Weiner, S. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 6048–6053. (5) Wang, R. Z.; Addadi, L.; Weiner, S. Philos. Trans. R. Soc., B 1997, 352, 469–480. (6) Lowenstam, H. A.; Weiner, S.Biomineralization and Biological Metal Accumulation, Biological and Geological Perspectives. In Mineralization by Organisms and the Evolution of Biomineraliza- tion; D. Reidel Publishing Company: Renesse, The Netherlands, 1983; pp 191-204. (7) Ma, Y.; Cohen, S. R.; Addadi, L.; Weiner, S. Adv. Mater. 2008, 20, 1555–1559. (8) Albeck, S.; Aizenberg, J.; Addadi, L.; Weiner, S. J. Am. Chem. Soc. 1993, 115, 11691–11697. (9) Goldsmith, J. R.; Graf, D. L.; Heard, H. C. Am. Mineral. 1961, 46, 453–459. (10) Kitano, Y.; Hood, D. W. J. Oceanogr. Soc. Jpn. 1962, 18(3), 141– 145. (11) Raz, S.; Weiner, S.; Addadi, L. Adv. Mater. 2000, 12(1), 38–42. (12) Loste, E.; Wilson, R. M.; Seshadri, R.; Meldrum, F. C. J. Cryst. Growth 2003, 254, 206–218.