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Controlled Crystallization and Transformation of Carbonate Minerals with Dumbbell-like Morphologies on Bacterial Cell Templates

Published online by Cambridge University Press:  10 February 2020

Chonghong Zhang ,
Fuchun Li ,
Jun Sun  and
Jiejie Lv
Chonghong Zhang
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing210095, China
Fuchun Li*
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing210095, China
Jun Sun
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing210095, China
Jiejie Lv
Affiliation:
College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing210095, China
*
*Author for correspondence: Fuchun Li, E-mail: [email protected]
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Abstract

Research on the biogenic-specific polymorphism and morphology of carbonate has been gaining momentum in the fields of biomineralization and industrial engineering in recent years. We report the nucleation of carbonate particles on bacterial cell templates to produce a novel dumbbell-like morphology which was assembled by needle-like crystals of magnesium calcite or aragonite radiating out from both ends of the template bacterium. Mature dumbbell-like structures had a tendency to break apart in the central template region, which was made up mostly of weak amorphous carbonate. Further crystal growth, especially at the template region, transformed the broken pieces into spherulites. Rod-like cell templates were essential for the formation of dumbbell-like morphologies, and we propose a possible formation mechanism of the dumbbell-like morphology. Our findings provide new perspectives on the morphological formation mechanism in biomineralization systems and may have a potential significance in assembling composite materials suitable for industrial applications.

Keywords

bacteriacarbonatecrystal growthdumbbell-like morphologynucleation template
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 26 , Issue 2 , April 2020 , pp. 275 - 286
Copyright
Copyright © Microscopy Society of America 2020

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References

Al-Thawadi, SM (2011). Ureolytic bacteria and calcium carbonate formation as a mechanism of strength enhancement of sand. J Adv Sci Eng Res 1, 98–114.Google Scholar
Azulay, DN, Abbasi, R, Ben Simhon Ktorza, I, Remennik, S, Reddy, MA & Chai, L (2018). Biopolymers from a bacterial extracellular matrix affect the morphology and structure of calcium carbonate crystals. Cryst Growth Des 18, 5582–5591.CrossRefGoogle Scholar
Braissant, O, Cailleau, G, Dupraz, C & Verrecchia, EP (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
Buczynski, C & Chafetz, HS (1991). Habit of bacterially induced precipitates of calcium carbonate and the influence of medium viscosity on mineralogy. J Sediment Res 61, 226–233.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
Cölfen, H (2003). Precipitation of carbonates: Recent progress in controlled production of complex shapes. Curr Opin Colloid Interface Sci 8, 23–31.CrossRefGoogle Scholar
Cui, J, Kennedy, JF, Nie, J & Ma, G (2015). Co-effects of amines molecules and chitosan films on in vitro calcium carbonate mineralization. Carbohydr Polym 133, 67–73.CrossRefGoogle ScholarPubMed
D'Souza, S, Alexander, C, Carr, S, Waller, A, Whitcombe, M & Vulfson, E (1999). Directed nucleation of calcite at a crystal-imprinted polymer surface. Nature 398, 312.CrossRefGoogle Scholar
Ferris, FG, Thompson, JB & Beveridge, TJ (1997). Modern freshwater microbialites from Kelly Lake, British Columbia, Canada. Palaios 12, 213–219.CrossRefGoogle Scholar
Fu, G, Valiyaveettil, S, Wopenka, B & Morse, DE (2005). CaCO3 biomineralization: Acidic 8-kDa proteins isolated from aragonitic abalone shell nacre can specifically modify calcite crystal morphology. Biomacromolecules 6, 1289–1298.CrossRefGoogle ScholarPubMed
Gilis, M, Meibom, A, Domart-Coulon, I, Grauby, O, Stolarski, J & Baronnet, A (2014). Biomineralization in newly settled recruits of the scleractinian coral Pocillopora damicornis. J Morphol 275, 1349–1365.CrossRefGoogle ScholarPubMed
Griesshaber, E, Kelm, K, Sehrbrock, A, Mader, W, Mutterlose, JR, Brand, U & Schmahl, WW (2009). Amorphous calcium carbonate in the shell material of the brachiopod Megerlia truncata. Eur J Mineral 21, 715–723.CrossRefGoogle Scholar
Guo, W, Ma, H, Li, F, Jin, Z, Li, J, Ma, F & Wang, C (2013). Citrobacter sp. strain GW-M mediates the coexistence of carbonate minerals with various morphologies. Geomicrobiol J 30, 749–757.CrossRefGoogle Scholar
Han, Z, Meng, R, Yan, H, Zhao, H, Han, M, Zhao, Y, Sun, B, Sun, Y, Wang, J & Zhuang, D (2017). Calcium carbonate precipitation by Synechocystis sp. PCC6803 at different Mg/Ca molar ratios under the laboratory condition. Carbonate Evaporite 32, 561–575.CrossRefGoogle Scholar
Kato, T, Sugawara, A & Hosoda, N (2002). Calcium carbonate–organic hybrid materials. Adv Mater 14, 869–877.3.0.CO;2-E>CrossRefGoogle Scholar
Kontrec, J, Ukrainczyk, M, Džakula, BN & Kralj, D (2013). Precipitation and characterization of hollow calcite nanoparticles. Cryst Res Technol 48, 622–626.Google Scholar
Langmuir, D (1997). Aqueous Environmental. Upper Saddle River, NJ: Geochemistry Prentice Hall.Google Scholar
Lian, B, Hu, Q, Chen, J, Ji, J & Teng, HH (2006). Carbonate biomineralization induced by soil bacterium Bacillus megaterium. Geochim Cosmochim Acta 70, 5522–5535.CrossRefGoogle Scholar
Liu, D & Yates, MZ (2006). Formation of rod-shaped calcite crystals by microemulsion-based synthesis. Langmuir 22, 5566–5569.CrossRefGoogle ScholarPubMed
Long, X, Ma, Y & Qi, L (2014). Biogenic and synthetic high magnesium calcite—A review. J Struct Biol 185, 1–14.CrossRefGoogle ScholarPubMed
Lv, JJ, Ma, F, Li, FC, Zhang, CH & Chen, JN (2017). Vaterite induced by Lysinibacillus sp. GW-2 strain and its stability. J Struct Biol 200, 97–105.CrossRefGoogle ScholarPubMed
Maeda, H & Kasuga, T (2006). Preparation of poly (lactic acid) composite hollow spheres containing calcium carbonates. Acta Biomater 2, 403–408.CrossRefGoogle ScholarPubMed
Mantilaka, MMMGPG, Pitawala, HMTGA, Rajapakse, RMG, Karunaratne, DGGP & Upul Wijayantha, KG (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, Brasier, A, Vonhof, H, Prior, T, Fellows, S, Reijmer, J, Billing, I & Pedley, H (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
Naka, K & Chujo, Y (2001). Control of crystal nucleation and growth of calcium carbonate by synthetic substrates. Chem Mater 13, 3245–3259.CrossRefGoogle Scholar
Nishino, Y, Oaki, Y & Imai, H (2008). Magnesium-mediated nanocrystalline mosaics of calcite. Cryst Growth Des 9, 223–226.CrossRefGoogle Scholar
Oral, ÇM & Ercan, B (2018). Influence of pH on morphology, size and polymorph of room temperature synthesized calcium carbonate particles. Powder Technol 339, 781–788.CrossRefGoogle Scholar
Pokroy, B, Fitch, AN, Marin, F, Kapon, M, Adir, N & Zolotoyabko, E (2006). Anisotropic lattice distortions in biogenic calcite induced by intra-crystalline organic molecules. J Struct Biol 155, 96–103.CrossRefGoogle ScholarPubMed
Raz, S, Weiner, S & Addadi, L (2000). Formation of high-magnesian calcites via an amorphous precursor phase: Possible biological implications. Adv Mater 12, 38–42.3.0.CO;2-I>CrossRefGoogle Scholar
Rivadeneyra, M, 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
Sánchez-Navas, A, Martín-Algarra, A, Rivadeneyra, MaA, Melchor, S & Martín-Ramos, JD (2009). Crystal-growth behavior in Ca–Mg carbonate bacterial spherulites. Cryst Growth Des 9, 2690–2699.CrossRefGoogle Scholar
Sánchez-Román, M, Romanek, CS, Fernández-Remolar, DC, Sánchez-Navas, A, McKenzie, JA, Pibernat, RA & Vasconcelos, C (2011). Aerobic biomineralization of Mg-rich carbonates: Implications for natural environments. Chem Geol 281, 143–150.CrossRefGoogle Scholar
Schmahl, WW, Griesshaber, E, Neuser, R, Lenze, A, Job, R & Brand, U (2004). The microstructure of the fibrous layer of terebratulide brachiopod shell calcite. Eur J Mineral 16, 693–697.CrossRefGoogle Scholar
Schultze-Lam, S, Fortin, D, Davis, B & Beveridge, T (1996). Mineralization of bacterial surfaces. Chem Geol 132, 171–181.CrossRefGoogle Scholar
Su, M, Han, J, Li, Y, Chen, J, Zhao, Y & Chadwick, K (2015). Ultrasonic crystallization of calcium carbonate in presence of seawater ions. Desalination 369, 85–90.CrossRefGoogle Scholar
Terada, T, Yamabi, S & Imai, H (2003). Formation process of sheets and helical forms consisting of strontium carbonate fibrous crystals with silicate. J Cryst Growth 253, 435–444.CrossRefGoogle Scholar
Wacey, D, Wright, DT & Boyce, AJ (2007). A stable isotope study of microbial dolomite formation in the Coorong Region, South Australia. Chem Geol 244, 155–174.CrossRefGoogle Scholar
Walker, JM, Marzec, B, Lee, RB, Vodrazkova, K, Day, SJ, Tang, CC, Rickaby, RE & Nudelman, F (2019). Polymorph selectivity of coccolith-associated polysaccharides from gephyrocapsa oceanica on calcium carbonate formation in vitro. Adv Funct Mater 29, 1807168.CrossRefGoogle Scholar
Warthmann, R, Van Lith, Y, Vasconcelos, C, McKenzie, JA & Karpoff, AM (2000). Bacterially induced dolomite precipitation in anoxic culture experiments. Geology 28, 1091–1094.2.0.CO;2>CrossRefGoogle Scholar
Xie, A-J, Shen, Y-H, Zhang, C-Y, Yuan, Z-W, Zhu, X-M & Yang, Y-M (2005). Crystal growth of calcium carbonate with various morphologies in different amino acid systems. J Cryst Growth 285, 436–443.CrossRefGoogle Scholar
Xu, C, Zhang, S, Chuang, C-y, Miller, EJ, Schwehr, KA & Santschi, PH (2011). Chemical composition and relative hydrophobicity of microbial exopolymeric substances (EPS) isolated by anion exchange chromatography and their actinide-binding affinities. Mar Chem 126, 27–36.CrossRefGoogle Scholar
Yan, GW, Huang, JH, Zhang, JF & Qian, CJ (2008). Aggregation of hollow CaCO3 spheres by calcite nanoflakes. Mater Res Bull 43, 2069–2077.CrossRefGoogle Scholar
Yoshimura, T, Tamenori, Y, Suzuki, A, Kawahata, H, Iwasaki, N, Hasegawa, H, Nguyen, LT, Kuroyanagi, A, Yamazaki, T & Ohkouchi, N (2017). Altervalent substitution of sodium for calcium in biogenic calcite and aragonite. Geochim Cosmochim Acta 202, 21–38.CrossRefGoogle Scholar
Zhang, Y & Dawe, RA (2000). Influence of Mg2+ on the kinetics of calcite precipitation and calcite crystal morphology. Chem Geol 163, 129–138.CrossRefGoogle Scholar
Zhang, C, Li, F, Li, X, Li, L & Liu, L (2018). The roles of Mg over the precipitation of carbonate and morphological formation in the presence of Arthrobacter sp. strain MF-2. Geomicrobiol J 35, 545–554.CrossRefGoogle Scholar
Zhang, C, Lv, J, Li, F & Li, X (2017). Nucleation and growth of Mg-calcite spherulites induced by the bacterium Curvibacter lanceolatus strain HJ-1. Microsc Microanal 23, 1189–1196.CrossRefGoogle ScholarPubMed
Zhao, L & Wang, J (2012). Biomimetic synthesis of hollow microspheres of calcium carbonate crystals in the presence of polymer and surfactant. Colloids Surf., A 393, 139–143.CrossRefGoogle Scholar
Zhong, C & Chu, CC (2010). On the origin of amorphous cores in biomimetic CaCO3 spherulites: New insights into spherulitic crystallization. Cryst Growth Des 10, 5043–5049.CrossRefGoogle Scholar
Zhou, G-T, Guan, Y-B, Yao, Q-Z & Fu, S-Q (2010). Biomimetic mineralization of prismatic calcite mesocrystals: Relevance to biomineralization. Cheml Geol 279, 63–72.CrossRefGoogle Scholar