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Nucleation and Growth of Mg-Calcite Spherulites Induced by the Bacterium Curvibacter lanceolatus Strain HJ-1

Published online by Cambridge University Press:  04 December 2017

Chonghong Zhang ,
Jiejie Lv ,
Fuchun Li  and
Xuelin Li
Chonghong Zhang
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China
Jiejie Lv
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China
Fuchun Li*
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China
Xuelin Li
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China
*
*Corresponding author. fchli@njau.edu.cn
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Abstract

Calcite spherulites have been observed in many laboratory experiments with different bacteria, and spherulitic growth has received much interest in mineralogy research. However, the nucleation and growth mechanism, as well as geological significance of calcite spherulites in solution with bacteria is still unclear. Herein, spherulites composed of an amorphous core, a Mg-calcite body and an organic film were precipitated by the Curvibacter lanceolatus HJ-1 bacterial strain in a solution with a molar Mg/Ca ratio of 3. Based on the results, we provide a possible mechanism for the biomineralization of Mg-calcite spherulites. First, amorphous calcium carbonate particles are deposited and aggregated into a stable sphere-like core in combination with organic molecules. The core then acts as the nucleus of spherulitic radial growth. Finally, the organic film grows on the surface of Mg-calcite spherulites as a result of bacterial metabolism and calcification. These findings provide insight into the growth mode and crystallization of biogenic spherulites during biomineralization, and are of significance in the application of novel biological materials.

Keywords

bacteriaMg-calciteACCspherulitegrowth
Type
Biological Science Applications
Information
Microscopy and Microanalysis , Volume 23 , Issue 6 , December 2017 , pp. 1189 - 1196
Copyright
© Microscopy Society of America 2017 

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References

Addadi, L., Raz, S. & Weiner, S. (2003). Taking advantage of disorder: Amorphous calcium carbonate and its roles in biomineralization. Adv Mater 15, 959–970.CrossRefGoogle Scholar
Aizenberg, J., Weiner, S. & Addadi, L. (2003). Coexistence of amorphous and crystalline calcium carbonate in skeletal tissues. Connect Tissue Res 44, 20–25.CrossRefGoogle ScholarPubMed
Beck, R. & Andreassen, J.P. (2010a). The onset of spherulitic growth in crystallization of calcium carbonate. J Cryst Growth 312, 2226–2238.CrossRefGoogle Scholar
Beck, R. & Andreassen, J.P. (2010b). Spherulitic growth of calcium carbonate. Cryst Growth Des 10, 2934–2947.CrossRefGoogle Scholar
Beniash, E., Aizenberg, J., Addadi, L. & Weiner, S. (1997). Amorphous calcium carbonate transforms into calcite during sea urchin larval spicule growth. Proc R Soc Lond B Biol Sci 264, 461–465.CrossRefGoogle Scholar
Benzerara, K., Menguy, N., Lopez-Garcia, P., Yoon, T.H., Kazmierczak, J., Tyliszczak, T., Guyot, F. & Brown, G.E. Jr. (2006). Nanoscale detection of organic signatures in carbonate microbialites. Proc Natl Acad Sci 103, 9440–9445.CrossRefGoogle ScholarPubMed
Bischoff, W.D., Bishop, F.C. & Mackenzie, F.T. (1983). Biogenically produced magnesian calcite: inhomogeneities in chemical and physical properties; comparison with synthetic phases. Am Mineral 68, 1183–1188.Google Scholar
Blanco-Ameijeiras, S., Lebrato, M., Stoll, H.M., Iglesias-Rodrihuez, M.D., Mendez-Vicente, A., Sett, S., Muller, M.N., Oschlies, A. & Schulz, K.G. (2012). Removal of organic magnesium in coccolithophore calcite. Geochim Cosmochim Acta 89, 226–239.CrossRefGoogle Scholar
Braissant, O., Cailleau, G., Dupraz, C. & Verrecchia, E.P. (2003). Bacterially induced mineralization of calcium carbonate in terrestrial environments: The role of exopolysaccharides and amino acids. J Sediment Res 73, 485–490.CrossRefGoogle Scholar
Cantaert, B., Verch, A., Kim, Y.Y., Ludwig, H., Paunov, V.N., Kroger, R. & Meidrum, F.C. (2013). Formation and structure of calcium carbonate thin films and nanofibers precipitated in the presence of poly (allylamine hydrochloride) and magnesium ions. Chem Mater 25, 4994–5003.CrossRefGoogle ScholarPubMed
Castanier, S., Le Metayer-Levrel, G. & Perthuisot, J.P. (2000). Bacterial roles in the precipitation of carbonate minerals. In Microbial Sediments (pp. 32–39. Berlin/Heidelberg: Springer.CrossRefGoogle Scholar
Chen, T., Neville, A. & Yuan, M. (2006). Influence of Mg2+ on CaCO3 formation—Bulk precipitation and surface deposition. Chem Eng Sci 61, 5318–5327.CrossRefGoogle Scholar
Declet, A., Reyes, E. & Suárez, O.M. (2016). Calcium carbonate precipitation: A review of the carbonate crystallization process and applications in bioinspired composites. Rev Adv Mater Sci 44, 87–107.Google Scholar
Della Porta, G. (2015). Carbonate Build-Ups in Lacustrine, Hydrothermal and Fluvial Settings: Comparing Depositional Geometry, Fabric Types and Geochemical Signature. London: Geological Society, Special Publications 418, 17–68.CrossRefGoogle Scholar
Ercole, C., Cacchio, P., Botta, A.L., Centi, V. & Lepidi, A. (2007). Bacterially induced mineralization of calcium carbonate: The role of exopolysaccharides a capsular polysaccharides. Microsc Microanal 13, 42–50.CrossRefGoogle ScholarPubMed
Goldenfeld, N. (1987). Theory of spherulitic crystallization. J Cryst Growth 84, 601–608.CrossRefGoogle Scholar
Gránásy, L., Pusztai, T., Tegze, G., Warren, J.A. & Douglas, J.F. (2005). Growth and form of spherulites. Phys Rev E 72, 011605.CrossRefGoogle ScholarPubMed
Jayaraman, A., Subramanyam, G., Sindhu, S., Ajikumar, P.K. & Valiyaveettil, S. (2007). Biomimetic synthesis of calcium carbonate thin films using hydroxylated poly (methylmethacrylate) (PMMA) template. Cryst Growth Des 7, 142–146.CrossRefGoogle Scholar
Khan, S.R. (1997). Calcium phosphate/calcium oxalate crystal association in urinary stones: Implications for heterogeneous nucleation of calcium oxalate. J Urol 157, 376–383.CrossRefGoogle ScholarPubMed
Kitamura, M. (2001). Crystallization and transformation mechanism of calcium carbonate polymorphs and the effect of magnesium ion. J Colloid Interf Sci 236, 318–327.CrossRefGoogle ScholarPubMed
Kontrec, J., Ukrainczyk, M., Džakula, B.N. & Kralj, D. (2013). Precipitation and characterization of hollow calcite nanoparticles. Cryst Res Technol 48, 622–626.CrossRefGoogle Scholar
Le Metayer-Levrel, G., Castanier, S., Orial, G., Loubierec, J.-F. & Perthuisota, J.-P. (1999). Applications of bacterial carbonatogenesis to the protection and regeneration of limestones in buildings and historic patrimony. Sediment Geol 126, 25–34.CrossRefGoogle Scholar
Li, T., Hao, L., Du, C. & Wang, Y. (2017). Synthesis of magnesium-doped calcium carbonate microcapsules through yeast-regulated mineralization. Mater Lett 193, 38–41.CrossRefGoogle Scholar
Li, L., Li, F., Liu, L., Zhang, C. & Lv, J. (2017). Aragonite formation induced by strain HJ-1 in low Mg/Ca condition. Acta Microbiol Sin 57, 434–446. (in Chinese).Google Scholar
Lian, B., Hu, Q., Chen, J., Ji, J. & Teng, H.H. (2006). Carbonate biomineralization induced by soil bacterium Bacillus megaterium . Geochim Cosmochim Acta 70, 5522–5535.CrossRefGoogle Scholar
Lors, C., Ducasse-Lapeyrusse, J., Gagné, R. & Damidot, D. (2017). Microbiologically induced calcium carbonate precipitation to repair microcracks remaining after autogenous healing of mortars. Construction Build Mater 141, 461–469.CrossRefGoogle Scholar
Magill, J.H. (2001). Review spherulites: A personal perspective. J Mater Sci 36, 3143–3164.CrossRefGoogle Scholar
Mantilaka, M., Pitawala, H., Rajapakse, R., Karunaratne, D. & Upul Wijayantha, K.G. (2014). Formation of hollow bone-like morphology of calcium carbonate on surfactant/polymer templates. J Cryst Growth 392, 52–59.CrossRefGoogle Scholar
Mercedes-Martín, R., Rogerson, M.R., Brasier, A.T., Vonhof, H.B., Prior, T.J., Fellows, S.M., Reijmer, J.J.G., Billing, I. & Pedley, H.M. (2016). Growing spherulitic calcite grains in saline, hyperalkaline lakes: Experimental evaluation of the effects of Mg-clays and organic acids. Sediment Geol 335, 93–102.CrossRefGoogle Scholar
Ocaña, M., Rodriguez-Clemente, R. & Serna, C.J. (1995). Uniform colloidal particles in solution: Formation mechanisms. Adv Mater 7, 212–216.CrossRefGoogle Scholar
Rivadeneyra, M.A., Delgado, G., Ramos-Cormenzana, A. & Delgado, R. (1998). Biomineralization of carbonates by Halomonas eurihalina in solid and liquid media with different salinities: crystal formation sequence. Res Microbiol 149, 277–287.CrossRefGoogle ScholarPubMed
Rodriguez-Navarro, C., Jimenez-Lopez, C., Rodriguez-Navarro, A., Gonzalez-Muñoz, M.T. & Rodriguez-Gallego, M. (2007). Bacterially mediated mineralization of vaterite. Geochim Cosmochim Acta 71, 1197–1213.CrossRefGoogle Scholar
Rodriguez-Navarro, C., Rodriguez-Gallego, M., Chekroun, K.B. & Gonzalez-Munoz, M.T. (2003). Conservation of ornamental stone by myxococcus xanthus-induced carbonate biomineralization. Appl Environ Microbiol 69, 2182–2193.CrossRefGoogle ScholarPubMed
Sánchez-Navas, A., Martín-Algarra, A., Rivadeneyra, M.A., Melchor, S. & Martín-Ramos, J.D. (2009). Crystal-growth behavior in Ca-Mg carbonate bacterial spherulites. Cryst Growth Des 9, 2690–2699.CrossRefGoogle Scholar
Wang, T., Cölfen, H. & Antonietti, M. (2005). Nonclassical crystallization: Mesocrystals and morphology change of CaCO3 crystals in the presence of a polyelectrolyte additive. J Am Chem Soc 127, 3246–3247.CrossRefGoogle ScholarPubMed
Wohlrab, S., Cölfen, H. & Antonietti, M. (2005). Crystalline, porous microspheres made from amino acids by using polymer-induced liquid precursor phases. Angewandte Chemie Int Edn 44, 4087–4092.CrossRefGoogle ScholarPubMed
Wright, D.T. & Wacey, D. (2005). Precipitation of dolomite using sulphate-reducing bacteria from the Coorong Region, South Australia: Significance and implications. Sedimentology 52, 987–1008.Google Scholar
Xu, Q., Zhang, C., Li, F., Ma, F., Guo, W., Li, X., Li, L. & Liu, L. (2017). Arthrobacter sp. strain MF-2 induces High-Mg calcite formation: Mechanism and implications for carbon fixation. Geomicrobiology J 34, 157–165.CrossRefGoogle Scholar
Xue, Z., Hu, B., Dai, S., Jiang, X., Wu, S. & Du, Z. (2011). Crystallization and self-assembly of calcium carbonate under albumin Langmuir monolayers. Mater Chem Phys 129, 315–321.CrossRefGoogle Scholar
Yan, G., Huang, J., Zhang, J. & Qian, C. (2008). Aggregation of hollow CaCO3 spheres by calcite nanoflakes. Mater Res Bull 43, 2069–2077.CrossRefGoogle Scholar
Yang, X., Xu, G., Chen, Y., Liu, T., Mao, H., Sui, W., Ao, M. & He, F. (2010). The influence of O-carboxymethylchitosan on the crystallization of calcium carbonate. Powder Technol 204, 228–235.CrossRefGoogle Scholar
Yoshimura, T., Tamenori, Y., Suzuki, A., Kawahata, H., Iwasaki, N., Hasegawa, H., Nguyen, L.T., Kuroyanagi, A., Yamazaki, T., Kuroda, J. & Ohkouchi, N. (2017). Altervalent substitution of sodium for calcium in biogenic calcite and aragonite. Geochim Cosmochim Acta 202, 21–38.CrossRefGoogle Scholar
Zhang, Z., Yang, B., Tang, H., Chen, X. & Wang, B. (2015). High-yield synthesis of vaterite CaCO3 microspheres in ethanol/water: Structural characterization and formation mechanisms. J Mater Sci 50, 5540–5548.CrossRefGoogle Scholar
Zhong, C. & Chu, C.C. (2010). On the origin of amorphous cores in biomimetic CaCO3 spherulites: New insights into spherulitic crystallization. Cryst Growth Des 10, 5043–5049.CrossRefGoogle Scholar
Zhu, L., Zhao, Q., Zheng, X. & Xie, Y. (2006). Formation of star-shaped calcite crystals with Mg2+ inorganic mineralizer without organic template. J Solid State Chem 179, 1247–1252.CrossRefGoogle Scholar