Coral Mineralization Inspired CaCO3 Deposition via CO2

Jan 5, 2010 - ABSTRACT: We report coral-inspired calcium carbonate deposition via sequestration of CO2 directly from the atmosphere. We observed that ...
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DOI: 10.1021/cg9012075

Coral Mineralization Inspired CaCO3 Deposition via CO2 Sequestration from the Atmosphere

2010, Vol. 10 851–855

Shichoon Lee, Jong-Hwan Park, Donghoon Kwak, and Kilwon Cho* Department of Chemical Engineering, Pohang University of Science and Technology, Pohang, 790-784, Korea Received October 1, 2009

ABSTRACT: We report coral-inspired calcium carbonate deposition via sequestration of CO2 directly from the atmosphere. We observed that a CaCl2 solution containing basic components and carbonic anhydrase induced aragonitic spherulites and acicular morphologies of CaCO3 at the air/solution interface, through the reaction of calcium ions with CO2 dissolved directly from the atmosphere; the resulting crystalline aragonite architectures were very similar to those in scleractinian corals. The addition of an anionic polymer enhanced deposition of CaCO3 at the air/solution interface, which was accompanied by morphological changes including coated spherulites; tabular, cone-shaped, and nanofibrillar calcites; and amorphous calcium carbonate. These architectures are abundant in corals in nature, and the results thus suggest that CaCO3 deposition via CO2 sequestration from the atmosphere, using a solution containing a basic component, carbonic anhydrase, and an anionic polymer, emulates coral mineralization. This study of abiotic mineralization can be used as a tool for understanding coral mineralization in nature, and also has implications for CO2 capture from the atmosphere.

Introduction Organisms make extensive use of calcium carbonate (CaCO3), one of the most abundant minerals in nature, as a structural or protective material. Calcium carbonate has been a focus substance for the storage of CO2, the greenhouse gas primarily responsible for global warming.1 Reef corals have attracted attention because approximately 90% of their biological carbonate is derived from ambient CO2 by gas exchange,2 whereas in most air-breathing animals that is from respired CO2. Coral calcification is distinctive because it is similar to abiotic mineralization, occurs fast, and involves rapid aragonite supersaturation at the calcification site, the deposition of aragonite fibers, and their organization into bundles. In coral mineralization, transporters such as proton and Ca2þ pumps, components involved in morphology control, and enzymes involved in hydration of CO2, are all considered to play essential roles. The hydration of CO2 gives rise to bicarbonate and a proton. Removing protons by proton pumping or with the use of buffering components facilitates the further decomposition of bicarbonates into carbonate ions, and enhances the reaction between calcium ions and carbonate ions. The transporters deliver calcium ions to the calcification site and expel protons generated by hydration of CO2; this results in an increase in pH, a rise in the supersaturation state of CaCO3, and precipitation of CaCO3.3-8 A notable feature of biomineralization is the involvement of biological macromolecules. Soluble anionic macromolecules including glycoproteins and phosphoproteins are known to function as inhibitors or stabilizers by binding precursor amorphous calcium carbonate (ACC), which acts as a template for transition of the ACC to structured crystals on the insoluble organic matrix.9 Genetic research has revealed that the enzyme carbonic anhydrase (CA), which is responsible for

hydration and dehydration of CO2, is involved in biomineralization of constitutive macromolecules in the relevant structures of the nacreous layer of oyster pearls,10 and in proteinmediated regulation of CaCO3 skeletogenesis in coralline sponges.11 Although its exact role is not yet known, CA is believed to function in transport of CO2 during the calcification process. Few genetic10,11 and physiological studies12 have been undertaken on the cellular process of aragonite formation in corals; such studies are difficult because of the complexity and symbiotic habit of the organisms. In vitro biomineralization studies have shown that even though aragonite calcium carbonates are abundant in corals, such calcium carbonates are formed only under a narrow range of experimental conditions13 or with use of specific additives.14 Here, we report the development of a simple experimental model system mimicking coral mineralization. We prepared a CaCl2 solution containing a basic component, CA, and a soluble anionic polymer; these are key inputs required for coral mineralization. The role of the basic component is to act as a proton pump capturing protons; CA is an enzyme involved in CO2 transport; and the anionic polymer acts as a morphology regulator. The system composed of these components was designed to induce CaCO3 nucleation and crystal growth at the air/solution interface, using CO2 sequestered from the atmosphere. With this system, we examined aragonite CaCO3 deposition at the air/solution interface and the evolution of various CaCO3 coral-like morphologies. Experimental Section

*To whom correspondence should be addressed. Tel.: 82-54-279-2270. Fax: 82-54-279-8298. E-mail: [email protected].

Calcium Carbonate Deposition. CaCO3 deposition was induced at the air/solution interface by the reaction of calcium ions in a CaCl2 solution with hydrated CO2 from the air, in the presence of bovine carbonic anhydrase (CA, Sigma-Aldrich) and basic components. The reaction vessel was a Petri dish (10 cm) containing 50 mL of 10 mM CaCl2 solution; the dish was covered with a lid containing several holes; and the solution was stirred at approximately 300 rpm using a magnetic stirrer.

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Figure 1. CaCO3 spherulitic aragonite morphologies formed at the air/solution interface in the presence of 10 μg/mL carbonic anhydrase and various basic components in 10 mM CaCl2. The microscope images are air-side views. Scale bar = 10 μm. (a) 100 mM ammonium hydroxide, 10 h. (b) 100 mM tris (hydroxyethyl) amino methane, 10 h. (c-f) Sequential morphological development in the presence of 10 mg/mL PEI2000 with aging time: (c) 4 h, (d) 5 h, (e) 10 h, and (f) 24 h. Solution Preparation. The CaCl2 solution provided calcium at the concentration usually found in seawater. The concentrations of ammonium hydroxide (AMH) and tris(hydroxyethyl)aminomethane (Tris) were both 100 mM. The polymeric basic components (polyethylenimine, PEI) used were water-soluble branched polymers with amine groups. Compounds of molecular weight 400 or 2000 g/mol (PEI400 and PEI2000, respectively; Sigma-Aldrich) were used at 10 mg/mL. Polyacrylic acid (PAA; molecular weight 2000 g/mol) was used to test the effect of an anionic component. Each solution was freshly prepared with Milli-Q water prior to use. The pH of solutions varied from 10.4 to 9.5 for PEI2000/CA, 11.3 to 10 for PEI400/CA, 11.5 to 8.7 for AMH/CA, and 10.8 to 9 for the Tris/CA solution after aging for 24 h. The pH declined by no more than 0.1 pH unit after addition of PAA. Sample Collection. For further characterization, CaCO3 formed at the air/solution interface was collected on silicon wafers cleaned with Piranha solution. The solution was decanted after the experimental period and the mass of the deposited CaCO3 was determined after vacuum drying. Calcium Carbonate Characterization. Polymorphs and crystal structures of the collected CaCO3 were investigated using field emission scanning electron microscopy (SEM, Hitachi S-4800), high-resolution transmission electron microscopy (HR-TEM, Jeol JFM-2100F), X-ray diffraction (XRD, θ/2θ scans at the 10C1 Beamline of the Pohang Accelerator Laboratory), and Raman spectroscopy (Renishaw System 3000), which is capable of focusing on crystals of interest.

Results and Discussion Coral mineralization was mimicked in a CaCl2 solution containing a basic component and CA, representing a proton pump and an enzyme for hydration of CO2, respectively (Supporting Information, Figure 1). The solution was exposed to the atmosphere, and CaCO3 formation was induced by the reaction of calcium ions in solution with carbonate ions derived from hydrated CO2 from the atmosphere. Almost no CaCO3 was observed at the air/solution interface or on the bottom of the Petri dish in the absence of a basic component. The amine groups of the basic component were protonated by continuous CO2 inflow and subsequent hydration, and the pH of the solution decreased with hydration of CO2. At a pH of

about 10 carbonate ions were readily generated during hydration of CO2, because of the buffering afforded by the basic components, and these ions subsequently reacted with calcium ions. The presence of CA induced deposition of CaCO3 in less than 10 h, both on the bottom of the dish and at the air/ solution interface. In buffer solutions of either AMH or Tris the presence of CA induced a film-like layer at the air/solution interface. No noticeable layer formed at the interface in the absence of CA. We observed that CA lowered surface tension at the air/solution interface (Supporting Information Figure 2), probably because of the enhanced hydration of CO2. The reduced surface tension implies that CA functionalizes the surface, which facilitates the heterogeneous nucleation15 that leads to CaCO3 deposition at the air/solution interface. This functionalized interface may act as an insoluble organic matrix or as a substrate for biomineralized structures. Many aggregated aragonitic spherulites were observed in the middle of the layer, and acicular aragonites occurred around the spherulites, as shown in Figure 1a,b. Similar fanlike morphologies of aragonitic spherulites have been reported in natural corals;16-18 the spherulites form because of an increase in the aragonite saturation state at the center of calcification sites, and the growth occurs in radial directions with a typical acicular form. In our system CO2 inflow was enhanced by stirring, and CO2 hydration was elevated in the presence of CA. Use of basic components caused more rapid generation of carbonate ions and subsequent reaction with calcium ions, resulting in aragonite supersaturation at the air/ solution interface. Supersaturation induced both outward and radial growth of acicular morphologies in the middle of the layer, leading to the formation of aragonitic spherulites. PEI is known as a proton sponge and can be used as a polymeric basic component. The sequential morphological developments that occurred with aging are shown in Figure 1c-f. Figure 1c shows several types of thin-film rosette precursors formed at the interface of the PEI2000/CA solution after 4 h of aging. Rosette bundles with many acicular fibers were apparent at 5 h, predominantly in the middle of the

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layer (Figure 1d). More developed and aggregated aragonite morphologies with larger petals were observed after 10 and 24 h of aging (Figure 1, panels e and f, respectively); these are similar to the diverging growth of aragonite fibers and the agglomerated morphology at the calcification center in symbiotic reef-building scleractinia.18 All spherulites and rosettes grown in solutions containing a basic component and CA were confirmed as aragonites by Raman spectroscopy (Supporting Information, Figure 3). Cohen18 showed that crystal morphologies change from tabular forms to spherulites with fine fibers as a function of increasing rate of crystal growth in coral skeletons. Crystals grown in PEI/CA were fine acicular aragonites and aggregates thereof (inset in Figure 1d), indicating that crystal growth was rapid. It is widely accepted that corals incorporate relatively low levels of organic material into their skeletons, but such materials do not affect the shape of the skeleton to the same degree as do mollusk nacre.18 Several studies have reported

Figure 2. Single-crystal CaCO3 examined by HR-TEM. Low magnification images by (a) SEM and (b) TEM. (c) Selected area electron diffraction (SAED) pattern at the zone axis [310]. (d) Experimental lattice spacing of aragonite grown in a solution containing 10 mg/mL PEI2000 and 10 μg/mL CA. Indices are based on JCPDS 41-1475: a = 4.961 A˚, b = 7.964 A˚, c = 5.738 A˚, R = β = γ = 90°. (e) Schematic drawing showing outgrowth of crystals along the c axis at the air/solution interface with aging time.

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interaction between carbonate ions and the amine groups of PEI, and the role of the process in generation of polymorphisms in less stable calcium carbonates, such as aragonite and vaterite.14 However, in addition to AMH and Tris, the PEI polymer acts as a basic buffer, which would function as a proton pump in coral mineralization and lead to the enhanced generation of carbonate ions, rather than regulating morphology by incorporation into minerals.19 The enhanced hydration by CA, and the proton pump activities of the basic component, may increase aragonite supersaturation conditions at the air/solution interface, resulting in production of both spherulitic aragonites and rosette aragonites. The fibers grew upward following CO2 inflow from the atmosphere. The selected area electron diffraction (SAED) pattern (Figure 2c) of a rosette petal grown in PEI2000/CA was shown by HR-TEM to be single-crystal aragonite. The measured d-spacings were 2.84 and 2.29 A˚, corresponding to the (002) and (130) planes, respectively. This indicates that the growth occurred in the direction of the longitudinal c-axis, as shown in Figure 2b-2e. Polyacrylic acid (PAA) has often been used in biomineralization studies, as a soluble anionic macromolecule.20,21 In the absence of PEI, a small amount of CaCO3 was deposited at the interface in the solution containing CA and PAA, at a much slower rate than seen when CA and PEI was present. The deposited material was characterized as an ACC by Raman spectroscopy and SEM (Supporting Information, Figure 4). A variety of coral-like or abiotic sedimentary morphologies were derived by addition of PAA to solutions containing PEI and CA (Figure 3). At a relatively low PAA concentration (10 μg/mL), a tabular calcitic morphology (Figure 3a) appeared at the air/solution interface, and was confirmed as single crystalline calcite, based on the SAED pattern and the XRD spectrum (Supporting Information, Figures 5 and 6a). The change of polymorph to calcite with addition of PAA is attributed to the binding of calcium ions to the anionic groups in PAA, which results in the nucleation and growth of calcite. Our results are consistent with the notion that calcite or vaterite polymorphs are induced principally in the presence of anionic macromolecules.22 The development of a tabular morphology with addition of a small amount of an anionic polymer was attributed to a reduction in counteranions (carbonate ions) relative to Ca2þ. In the absence of

Figure 3. CaCO3 morphologies formed at the air/solution interface with differing concentrations of poly(acrylic acid) (PAA) and various aging times. Carbonic anhydrase: 10 μg/mL; polyethylenimine (PEI): 10 mg/mL; CaCl2: 10 mM. The microscope images are air-side views. (a) 10 μg/mL PAA/ PEI2000, 10 h. (b) 30 μg/mL PAA/PEI2000, 24 h; upper inset: top view, lower inset: side view. (c) 50 μg/mL PAA/PEI2000, 24 h. (d) 100 μg/mL PAA/PEI2000, 24 h. (e) 10 μg/mL PAA/PEI400, 10 h. (f) 30 μg/mL PAA/PEI400, 24 h. (g) 50 μg/mL PAA/PEI400, 24 h. (h) 100 μg/mL PAA/PEI400, 24 h.

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sufficient anionic macromolecules to interact with all positively charged surfaces, growth in the diverse directions resulted, as reflected in the platelet morphology in deep waters of the marine environment, where the degree of CaCO3 supersaturation is low and crystal growth rates are thus slow.23 As the PAA concentration was increased to 30 μg/mL, cone-shaped superstructures (Figure 3b) with many small cones (lower inset, Figure 3b) formed in the PEI2000/CA solution; these are similar to Holocene composite crystals with smaller trigonal prisms.23 At 50 μg/mL PAA, prismatic superstructures aggregated with nanofibrillar bundles (some hollow, inset) and grew perpendicular to the air/solution interface, within 24 h (Figure 3c). These morphologies are very similar to those of aggregated nanofibers of BaSO4 grown in the presence of sodium polyacrylate.24 Addition of PAA at levels up to 100 μg/mL did not induce a nanofibrillarbundled morphology, and, by XRD and Raman spectroscopy (Supporting Information, Figures 4 and 6b) the disorganized growth that occurred at the interface over 24 h (Figure 3d) was characterized as a calcite with a large proportion of ACC. Morphologies changed depending on the molecular weight of the PEI added. At the interface of a solution containing PAA, CA, and PEI400, the film-like spherulites (confirmed as calcite by XRD; Supporting Information, Figure 6c) grew horizontally and were impinged upon by other spherulites, as shown in Figure 3e; this morphology coincides with that of ooids, which typically forms on the sea floor.23 With increasing concentration of PAA in the solution, cone shapes were apparent at 30 μg/mL (Figure 3f) and agglomerated cones consisting of nanofibrillar bundles appeared at 50 μg/mL (Figure 3g). Secondary geometries, including folding inside the cone, occurred at 100 μg/mL PAA (Figure 3h), which contrasts with the disorganized film that formed with addition of 100 μg/mL PAA to the PEI2000/CA solution (Figure 3d). However, the morphological developments seen using increasing PAA concentration resembled those observed with decreasing molecular weight of PEI. Thus, in PEI400/CA or PEI2000/CA solutions, the formation of film-like or tabular calcite was noted at a lower PAA concentration, and a coneshaped morphology and superstructures bundled with nanofibers (thus making the cones finer and aligned more perpendicularly to the interface) was observed with increasing PAA concentration. Changes in morphology with addition of anionic macromolecules have been discussed by several authors.9,20,21 The higher concentration of cations compared to anionic counterions, as occurred at early stages in our system, initially induces positively charged ACC nanoparticles on the surface, which might readily be bound to the carboxyl groups of PAA. These amorphous hybrid nanoparticles arrange to form nanofibers that aligned with the mesoscale assembly, resulting in bundled nanofiber structures. Our work shows that the concentration of anionic macromolecules bound to the Ca2þ-charged surface of the incipient ACC strongly influenced the resulting morphologies. This type of mineralization, with combined basic and anionic components, is analogous to biosilica formation in diatoms, involving a combination of phosphorylated anionic protein (silaffin-1A) with a long-chain polyamine.25 The cones shown in Figure 3 were not inverted, suggesting that cone growth was attributable to the continual inflow of CO2 from the atmosphere, as may explain growth of the rosette in Figure 1. The direction of crystal growth in precipitation of metal oxides is known to be controlled by the concentration of anionic surfactant and the ratio of cations to

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Figure 4. Amount of CaCO3 deposited as a function of PAA concentration and aging time. (a) CaCO3 deposition through reaction between calcium ions and CO2 dissolved from the air in a solution of 10 mg/mL of PEI2000, 10 mM CaCl2, and carbonic anhydrase (CA). Deposit quantities are the average of three tests, and the error bars indicate the standard deviation. (b) Film-like layers formed at the air/solution interface with combined addition of CA and PAA. A longer deposition induction time is required with the addition of PAA.

anions.9,23 The outgrowth direction of the cones in our experiment contrasts with the direction of calcite or vaterite outgrowth from in a premade supersaturated solution, where crystals grew downward as CO2 diffused from the solution to the interface.26,27 Figure 4 shows the amount of CaCO3 deposited over time in a solution of 10 mg/mL PEI2000 and 10 mM CaCl2 containing varying concentrations of PAA. In the solution containing PEI2000 and CA, 40 mg of CaCO3 was deposited, indicating that 80% of the added calcium ions were consumed by CO2 from the atmosphere (ignoring the amounts of additives and water incorporated). The addition of 10 μg/mL PAA reduced deposition to around 65% of that from the solution without PAA, and further addition of PAA (50 or 100 μg/mL) resulted in almost no deposition in 24 h (graph and Petri dish images, Figure 4). However, in the presence of PAA deposition increased to that seen without PAA after 100 h of aging, indicating the need for a longer induction time because of the presence of the anionic component. With increasing PAA concentration the presence of CA caused the layer at the air/solution interface to thicken over 100 h of aging time (Figure 4b, Supporting Information, Figure 7). These observations indicate that CA contributes to deposition of CaCO3 at a specific position (e.g., the calcification site), as suggested to explain involvement of CA in biomineralization.10,11,28 The above results show that PEI and PAA function as materials for the capture of CO2. Conclusion Coral mineralization was mimicked abiotically, and various coral-like CaCO3 architectures were formed by the reaction of calcium ions in solution and CO2 derived from

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the air. A CaCl2 solution containing CA and a basic buffer component resulted in formation of rosette aragonitic CaCO3 at the air/solution interface similar to those observed in scleractinian corals. The addition of an anionic component, at varying concentrations, to the solution gave rise to various coral-like morphologies, including coated spherulitic, coneshaped, and nanofibrillar calcites. This study has shown that a variety of coral-like architectures can be grown under atmospheric conditions, and the model system developed can be used in biomineralization studies. Acknowledgment. The authors thank Sungnam Kim for technical help with Raman spectroscopy. This work was supported by a grant from the Center for Nanostructural Materials Technology (M108KO010008-K1501-00810) under the 21st Century Frontier R&D Programs and the Korea Research Foundation Grant (KRF-2006-005-J01302). Supporting Information Available: Raman spectra, selected area electron diffraction pattern for the tabular morphology, X-ray diffraction information, a layer of calcium carbonates formed at the air/ solution interface and surface tension of solutions. This material is available free of charge via the internet at http://pubs.acs.org.

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