Direct Observations of the Occlusion of Soil Organic Matter within

Article Cite This: Environ. Sci. Technol. 2019, 53, 8097−8104

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Direct Observations of the Occlusion of Soil Organic Matter within Calcite Jialin Chi,† Wenjun Zhang,*,† Lijun Wang,*,† and Christine V. Putnis‡,§ †

College of Resources and Environment, Huazhong Agricultural University, Wuhan 430070, China Institut für Mineralogie, University of Münster, 48149 Münster, Germany § Department of Chemistry, Curtin University, Perth 6845, Australia ‡

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ABSTRACT: Global soil carbon cycling plays a key role in regulating and stabilizing the earth’s climate change because of soils with amounts of carbon at least three times greater than those of other ecological systems. Soil minerals have also been shown to underlie the persistence of soil organic matter (SOM) through both adsorption and occlusion, but the microscopic mechanisms that control the latter process are poorly understood. Here, using time-resolved in situ atomic force microscopy (AFM) to observe how calcite, a representative mineral in alkaline soils, interacts with humic substances, we show that following adsorption, humic substances are gradually occluded by the advancing steps of spirals on the calcite (1014) face grown in relatively high supersaturated solutions, through the embedment, compression, and closure of humic substance particles into cavities. This occlusion progress is inhibited by phytate at high concentrations (10−100 μM) due to the formation of phytate-Ca precipitates on step edges to prevent the step advancement, whereas phytate at relatively low concentrations (≤1 μM) and oxalate at high concentrations (100 μM) have little effect on this process. These in situ observations may provide new insights into the organo−mineral interaction, resulting in the incorporation of humic substances into minerals with a longer storage time to delay degradation in soils. This will improve our understanding of carbon cycling and immobilization in soil ecological systems.

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subsequent crystal growth, morphology, and structure.16−18 In addition to adsorption, evidence indicates that occlusion of organic matter into clay aggregates could further limit the enzymatic attack or oxygen diffusion to the site of microbial activity.19 Recently, Hernandez-Sorano et al.20 demonstrated the formation of organo−mineral microaggregates rather than mineral particles surrounded/adsorbed by organic debris using synchrotron-based infrared microspectroscopy. Moreover, the adsorbed organic substances may be incorporated and occluded into the minerals during their growth in supersaturated solutions in a local soil solution environment.21 The adsorption and occlusion process are complex and dynamic in natural soils due to the presence of various biomolecules such as phytate22,23 and oxalate24,25 that are widely distributed in soils with a concentration range of 0.1− 1000 and 1- 500 μM, respectively.22−25 They can dissolve the minerals through complexation and chelation with metal ions to release the organic matter or promote the dissolution of minerals and the transformation of adsorption/complexation

INTRODUCTION Global carbon cycling is a critical factor in controlling climate change,1,2 and soils are the main carbon sources because soil organic matter (SOM) contains more than three times as much organic carbon as that found in global vegetation and the atmosphere.3−5 Most soil carbon is derived from below-ground inputs and is transformed to carbon dioxide or methane as greenhouse gases.6 Thus, the stability of SOM plays an important role in influencing the exchange of carbon between soil and atmosphere.7,8 Much evidence has shown that its stability is dependent on physical, chemical, and biological controls over the decomposition progress.3,6,9 Among the above factors, soil minerals contribute to the stabilization of organic substances by the association of SOM and reactive mineral phases, as the adsorption affinity to minerals exceeds that of enzyme active sites to SOM. This leads to a slower SOM degradation on time scales from centuries to millennia.9−12 As the most reactive fraction of natural SOM in soils, humic substances are widely distributed in both acidic and alkaline soils and they can adsorb onto calcite or other carbonate minerals via electrostatic and van der Waals interactions, chelation, H-bonding, ligand exchange, and cation bridging.13−15 Humic substances can also interact with calcite after their adsorption on calcite and regulate the © 2019 American Chemical Society

Received: Revised: Accepted: Published: 8097

December 3, 2018 June 2, 2019 June 17, 2019 June 17, 2019 DOI: 10.1021/acs.est.8b06807 Environ. Sci. Technol. 2019, 53, 8097−8104

Article

Environmental Science & Technology

Figure 1. Kinetics of adsorption and occlusion of humin on a calcite (1014) face. In situ AFM deflection images of the (1014) cleavage surface of calcite, showing a rhombohedral spiral grown in a supersaturated solution at (A) σ = 1.196 (pH 8.3) and (B) σ = 0.140 (pH 8.3, step velocity, v+ and v− ≈ 0). (C) Following the injection of a supersaturated solution at σ = 0.140 (pH 8.3) in the presence of 10 mg/L humin, aggregated particles were formed on the calcite surface. (D−H) Enlarged rectangle taken from a dotted square in (C) showing that adsorbed humin particles are continuously occluded within calcite with time through layer-by-layer advancement of steps with increasing σ from 0.140 to 1.196 (pH 8.3). During this process, some gaps and cavities form in (F, G), and finally the cavities were closed to encapsulate the particles resulting in complete incorporation. (D’-H’) Height profiles of humin particles measured along the dashed lines in (D−H), showing the changes of corresponding particle heights during the occlusion process. Images A and B were collected in contact mode, and images C−H were collected in ScanAsyst mode.

to surface precipitation.22−26 Keiluweit et al.27 found that oxalate leads to the loss of organic matter due to the release of organic matter from minerals that undergo enhanced dissolution by oxalate. While these results have suggested that the occlusion process is involved in the mineral protection of SOM, details concerning this process after adsorption of humic substances on minerals, especially in the presence of other biomolecules, remain unclear. Specifically, a direct observation of the kinetic pathways and mechanisms of occlusion of SOM in the presence of organic acids or organophosphates at the calcite− fluid interface at microscopic levels is lacking. In this study, we chose calcite crystals, as they are major minerals in the Earth’s crust, especially in calcareous soils,28,29 and three typical humic substances including humic acid, fulvic acid, and humin. The occlusion of humic substances in the absence and presence of phytate or oxalate was investigated using in situ atomic force microscopy (AFM). To our knowledge, there has been no direct observation to image the occlusion process of SOM at the nanoscale. These in situ observations may provide insights into the stabilization, persistence, or decomposition of SOM at the mineral interface and inside minerals, and improve the mechanistic understanding of the role of soil minerals in carbon cycling.

Chemical Reagent, Shanghai) were used. Humin was extracted from soils (Sha Yang, Hubei) with NaOH and Na4P2O7,30 and then after discarding the supernatant, the dried precipitate was dissolved in ultrahigh pure water. In Situ AFM Imaging. Supersaturated calcite solutions at supersaturations (σ) of 0.140 and 1.196 were used in AFM experiments and the saturation index, σ is defined by σ = log a(Ca2+)a(CO32−)/Ksp, where a(Ca2+) and a(CO32−) are the activities of the calcium ion and carbonate ion, respectively, and Ksp (10−8.48)31 is the equilibrium solubility product of calcite. The activity ratio of Ca2+ to CO32− was 1.04 ± 0.01 by adjusting the solution concentrations of NaHCO3 and CaCl2, and the Davies equation was used to calculate ion activities. The solution pH was adjusted to 8.3 using 0.01 M NaOH, and the ionic strength (IS) of each solution was fixed to 0.11 M by NaCl. A NanoScope V-Multimode 8 AFM (Bruker, Santa Barbara, CA) equipped with a fluid cell sealed with an O-ring was used to perform the in situ AFM experiments, working in contact mode or ScanAsyst mode at a solution flow rate of 0.3 mL/ min. The images were collected using silicon nitride probes (Bruker, ScanAsyst-Fluid+ tips, spring constant of 0.7 N/m for ScanAsyst mode; DNP-10 tips, spring constant of 0.12−0.35 N/m for contact mode) with scan rates of 1−3 Hz. The mounted samples were first imaged in air, and then a supersaturated solution with respect to calcite (σ = 1.196) was injected over the calcite substrate. Later, a nearequilibrium supersaturated solution (σ = 0.140) in the presence of 10 mg/L humic acid, fulvic acid, or humin was passed over the calcite surface. After the adsorption of different humic substances, this highly supersaturated solution (σ =

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EXPERIMENTAL SECTION Calcite and Humic Substances. Freshly cleaved Iceland Spar calcite (1014) surfaces (Chihuahua, Mexico) were used for AFM experiments. Pure reaction grade humic acid (SigmaAldrich, St. Louis, Missouri) and fulvic acid (Shanghai Vita 8098

DOI: 10.1021/acs.est.8b06807 Environ. Sci. Technol. 2019, 53, 8097−8104

Article


When the supersaturated solution at σ = 1.196 was used again, the height of humin particles decreased with the spreading of steps, and the particles were gradually entrapped into calcite (Figures 1D−H, D’−H’, and S3). Some gaps and cavities were formed during the entrapment of humin particles (Figure 1F,G). Moreover, the cavities were gradually deepened to form internal cavities when the advancing steps crossed over the cavity edges, and these internal cavities may remain until the cavities get covered during the growth process (Figure S3). Finally, all the humin particles were finally incorporated into the calcite by the advancement of steps that covered the cavities (Figure 1H). Similar processes were observed on calcite with adsorbed fulvic acid or humic acid (Figure S4). This can be further confirmed by observing the dissolution of the newly forming calcite. Upon introduction of ultrapure water into the fluid cell, the top layers of the newly grown calcite rapidly dissolved, and the buried particles incorporated within the calcite were exposed (Figure S5A−E). Before and after the occlusion, the size of the particles decreased slightly (Figure S5F,G), suggesting that the particles possibly underwent lateral compression during the incorporation and occlusion. We further compared the time required for the complete incorporation of three humic substances within calcite by noting the burial times and measuring the height of 20 adsorbed particles of each humic substance. Then linear fitting for particle heights and the burial time of three types of humic substances was performed and the slopes were compared. The results showed a linear dependence of the incorporation time on the particle height. The slope of a plot of time vs incorporation in the presence of humin, fulvic acid, or humic acid was 7.37 ± 1.72, 8.12 ± 1.80, or 7.42 ± 2.37 min/nm, respectively (Figure 2). The three humic substances all have

1.196) was again injected to observe the occlusion process. Phytate and oxalate at 1−100 μM were chosen to study the influence of organophosphates and organic acids on the occlusion process and the step movement velocity through the measurements of v+ or v− as reported previously by RuizAgudo et al.32 The data were repeated at least three times with different crystals. NanoScope analysis software (Bruker) was used to analyze the images. X-ray Photoelectron Spectroscopy (XPS). Calcite crystals were reacted with 100 μM phytate in calcite supersaturated solutions (σ = 0.140 pH 8.3) for 12 h prior to XPS measurements to analyze the precipitate components using the XPS spectrometer (VG multilab 2000 equipment ThermoVG scientific, East Grinstead, West Sussex, U.K.).33 Briefly, the treated samples were analyzed with the excitation energy at 300 W and the C 1s peak was set to 284.6 eV for calibrating the binding energies. Data are analyzed by Thermal Advantage software (http://www.tainstruments.com) with the linearly subtracted background. Dynamic Light Scattering (DLS) and ζ Potential. Ten mg/L humic acid, fulvic acid, or humin was dissolved in a nearequilibrium solution supersaturated with respect to calcite (σ = 0.140, pH 8.3, 25 °C) for the measurement of particle sizes using DLS (Zatasizer Nano ZS90, Malvern, Worcestershire, U.K.); 10 mg/L humic acid, fulvic acid, or humin solutions were prepared at pH 8.3 for the measurement of ζ potential, and data were analyzed by Zetasizer software. Scanning Electron Microscopy (SEM). The calcite was placed in a beaker containing 10 mL of calcite supersaturated solutions (σ = 0.140) with 100 μM phytate for 12 h. The reacted calcite was sputter-coated with gold−palladium, placed on aluminum stubs, and examined by field-emission SEM (FEI SIRION 200) with an 5−20 kV accelerating voltage.

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RESULTS Occlusion of Humic Substance Particles on a Calcite (1014) Surface. In a supersaturated solution at σ = 1.196, the growing calcite hillocks (spiral growth) exhibited a typical rhombohedral geometry with obtuse and acute steps, one unit cell high (∼3.5 Å) on the exposed (1014) surface, observed in contact mode by in situ AFM (Figure 1A). Then, a nearequilibrium supersaturated solution (σ = 0.140, step advancement velocity v+ and v− ≈ 0. Figures 1B and S1) was flowed over the surface. Following the injection of this supersaturated solution (σ = 0.140) in the presence of 10 mg/L humin, humic acid, or fulvic acid, aggregated particles, with widths of 109.92 ± 2.08 nm (n = 40) (Figures 1C, S2A,A’), 41.28 ± 1.06 nm (n = 40) (Figure S2B,B’), and 60.36 ± 0.48 nm (n = 40) (Figure S2C,C’), respectively, and with heights of 10.25 ± 0.31 nm (n = 50) (Figure S2A,A’’), 2.13 ± 0.11 nm (n = 40) (Figure S2B,B’’) and 5.31 ± 0.06 nm (n = 40) (Figure S2C,C’’), respectively, formed on the calcite surface that was scanned in ScanAsyst mode to minimize the interactions of tip and particles. Moreover, we noted that the particle sizes measured by DLS were much larger than those measured by AFM in width and height measurements. This may result from a number of possible causes: the difference between the two methods for obtaining diameters because of the hydrodynamic diameter measured by DLS, or a surface-induced deaggregation phenomenon at the calcite surface or during solution flow in the tubing;34 the size trend, humin > fulvic acid > humic acid, was consistent via the two different methods (Figure S2D).

Figure 2. Relationship of particle heights and incorporation times within calcite for three humic substances, showing a linear dependence of incorporation time and particle height. The data were obtained by observing the burial time and measuring the height of 20 adsorbed particles of each humic substance. Then linear fitting for particle heights and the burial time of three types of humic substances was performed, and the slopes were compared. Slopes of the three lines do not exhibit significant differences at P < 0.01.

negative electrostatic properties (based on ζ potential analyses) due to their similar chemical components, such as carboxyl, phenolic, and hydroxyl groups. Thus, there was no significant difference in slopes in the time vs incorporation plot (at P < 0.01), suggesting that the occlusion time of all the humic substances is predominantly positively correlated to the particle size with the same occlusion mechanism. On the basis of the above observations, we, therefore, just chose humin as a representative humic substance with the greatest size of particles (Figure S2) for subsequent experiments. Roles of Phytate and Oxalate in the Occlusion Process. Phytate and oxalate are widely present in 8099


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Figure 3. Effect of low concentration of phytate (1 μM) on the occlusion process. (A, B) AFM images of humin adsorbed on a calcite surface to form particles (about 10 nm in height) after 20 min of exposure in a supersaturated solution (σ = 0.140, pH 8.3) in the presence of 10 mg/L humin. (C) No other new particles formed after 20 min of addition of 1 μM phytate in a supersaturated solution (σ = 0.140, pH 8.3). (D−F) After 60 min post injection of a highly supersaturated solution (σ = 1.196, pH 8.3), the adsorbed humin particles are gradually incorporated into the calcite crystal.

Figure 4. Inhibition effect of phytate at high concentration on the occlusion process. (A, B) Humin particles (about 4−13 nm in height) adsorbed on calcite after 20 min of exposure in a supersaturated solution (σ = 0.140, pH 8.3) in the presence of 10 mg/L humin. (C) Ten min after the introduction of 100 μM phytate in a supersaturated solution (σ = 0.140, pH 8.3), newly formed particles with (D) relatively small sizes of 2.43 ± 0.12 nm (n = 40) are rapidly adsorbed along step edges. (E−G) No step advancement in a high supersaturation solution (σ = 1.196, pH 8.3), inhibiting the occlusion progress. (H) Height profiles showing that there is no obvious change in the height of the same particles marked by circles I, II, and III in B (the particle height shown by the solid line in H) and G (the particle height shown by the dashed line in H) before and after the occlusion.

soils.22−25 Thus, we chose them to investigate their roles in modulating the occlusion of humin. When a supersaturated solution at σ = 0.140 in the presence of 1 μM phytate was injected over a calcite (1014) surface, no new particles were

formed on the calcite surface (Figures 3C and S7A), and the adsorbed humin particles could be occluded into the calcite at a higher supersaturation at σ = 1.196 (Figure 3D−F). However, when phytate concentrations were further increased 8100


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Environmental Science & Technology to 10−100 μM, in addition to larger humin particles (about 4− 13 nm) (Figures 4B,H and S7B), the newly formed particles with heights of about 2.4 nm were rapidly absorbed along step edges (Figures 4C,D, 5B,C and S7B,C). This resulted in no

step advancement even in a high supersaturation solution (σ = 1.196) (Figures 4E−G and S7B), thus inhibiting the occlusion progress, and humin particles maintained a constant size of about 4−13 nm (Figure 4H). We further analyzed components of adsorbed particles in the presence of phytate, and EDX spectra showed that the particles adsorbed on calcite consisted of Ca, O, C, and P (Figure S6). XPS results showed a clear peak at 135.3 eV for P2p (Figure 5D), which was identified as phosphate groups in calcium phytate.30 The other peaks at 132.1, 132.8 and 133.8 eV correspond to phosphate groups in pure phytate (Figure 5D).35,36 These results demonstrate the concentration-dependent modulation of phytate on the occlusion process, suggesting that phytate prevents the occlusion of humic substances at relatively high concentrations (10−100 μM) via a strong inhibition of step advancement, while at low concentrations (≤1 μM), this inhibitory effect is reduced allowing for increased step growth movement (Figure S8). Compared to phytate, no new particles were formed after the addition of 100 μM oxalate to a supersaturated solution at σ = 0.140 (Figures 6, S9, and S10B). This result is similar to that of low concentrations of phytate. After the injection of a high supersaturation solution (σ = 1.196) the adsorbed humin particles were gradually incorporated into the calcite (Figures 6 and S9). In addition, the step advancement velocities also decreased with an increase of oxalate concentrations, while the inhibitory effect is obviously weakened compared with that of phytate (Figure S8). This suggests that oxalate could not effectively influence the occlusion process even at high concentrations.

Figure 5. (A, B) In situ AFM height images showing the adsorption of particles on the step edges of a growing spiral in a supersaturated solution (σ = 0.140, pH 8.3) in the presence of 100 μM phytate. (C) Height distribution (2.45 ± 0.18 nm, n = 40) of particles. (D) Highresolution XPS spectra of the P2p of calcite crystallites reacted in a supersaturated solution (σ = 0.140, pH 8.3) in the presence of in 100 μM phytate for 12 h. A clear peak at 135.3 eV and the other smaller peaks at 132.1, 132.8, and 133.8 eV are identified to be phosphate groups in phytate-Ca or phosphate groups in pure phytate, respectively.

Figure 6. Effect of oxalate on the occlusion process. (A, B) AFM images of humin adsorbed on a calcite surface to form particles (about 10 nm in height) after 20 min of exposure in a supersaturated solution (σ = 0.140, pH 8.3) in the presence of 10 mg/L humin. (C) No other new particles were formed after 10 min of addition of 100 μM oxalate in a supersaturated solution (σ = 0.140, pH 8.3). (D, E) After 60 min post injection of a high supersaturated solution (σ = 1.196, pH 8.3), the adsorbed humin particles are gradually incorporated into a calcite spiral. (F) Height profiles along lines 1 → 2 and 3 → 4 showing that the same particle is gradually occluded. 8101


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DISCUSSION Adsorption. Humic substances can be regarded as supramolecular assemblies of different molecules,37 and their aggregation and deposition are dependent on the solution conditions38 through electrostatic and steric effects.13 In the present study, three humic substances, including humic acid, fulvic acid, and humin, in solutions supersaturated with respect to calcite at pH 8.3 (typical of carbonate-rich soils) exhibited spontaneous aggregation to form spherical particles (Figures 1C and S2). In alkaline solutions, the formation of the separated round-shaped structures is due to the deprotonation of the humic substance functional groups, contributing to the intra- and intermolecular electrostatic repulsive forces.39 The negatively charged spherical particles (Figure S2E), easily adsorb on the calcite surface with a positive ζ potential at pH 8.3.40 Moreover, humic substances contain various functional groups, including phenolic, carboxyl, carbonyl, and hydroxyl groups, that could also bind to the Ca2+ exposed at the step edges and crystal lattices of calcite to enhance the adsorption.13,18,41 Occlusion. All the adsorbed humic substances are gradually occluded by the advancing steps of spirals grown in a relatively high supersaturation solution through the three processes: (i) the advancing steps begin to cover and bury the particles, (ii) the particles are compressed and gaps and/or cavities form, and (iii) the cavities are ultimately closed. The whole burial process could generate local lattice strain through the micromechanical simulation outlined by Cho et al.21 and lattice strain also observed by Kim et al.42 via XRD analyses, and thus this local strain could result in gap formation. Moreover, the humic substances could be compressed during occlusion (Figure S5), as the modulus of humic substances is smaller than that of calcite. Therefore, lateral compression of humic substances by steps and the subsequent loss of associated water molecules and/or collapse of polymer chains may occur. Moreover, for any adsorbed particles with a larger modulus than that of calcite, this may favor perturbations of the growth layers.21,39,43 During the burial processes, the chemical components and surface electrostatic properties of the particles are important for effective occlusion.40,44−46 Qiu et al.47 found that osteopontin proteins remained on the (101) face of calcium oxalate monohydrate crystals without being incorporated into the crystal because of binding strength that is controlled by chemistry and steric conditions with respect to the terrace and steps of the crystal surface. Ning et al.40 also found that the presence of carboxyl-stabilized particles cannot be buried as the anionic component is an additional prerequisite. In our study, the three humic substances have negative surface electrostatic properties (Figure S2E) and similar functional groups,18,41 thus their burial process depends on the degree of supersaturation and particle size, leading to the similar values of the plotted slopes. The presence of phytate results in the concentrationdependent modulation of the occlusion process, preventing the occlusion at high concentrations (10−100 μM), and newly formed particles should be phytate-Ca precipitates based on XPS analyses. The main constituents of phytate in the solutions are H2Phy10−, H3Phy9−, and H4Phy8− at pH 8.348,49 that bind to step edges of calcite via electrostatic interactions between phosphate groups of phytate and Ca2+ ions.13 As DLS data of phytate in the specific solution conditions indicate no

formation of such particles shown on the step edges, it can be suggested that the particles were formed by surface precipitation along step edges (Figure 4B). Once the phytate-Ca nanoparticles/precipitates form along the step edges, step movement and propagation may be inhibited by the reduced possibility of the attachment of Ca2+ and CO32− ions from solution to the step edges via step pinning or lowering of supersaturation.50 This will lead to an obvious suppression of occlusion as observed in the AFM experiments. Moreover, phytate monomers/polymers probably existed on the surface, and they could be ignored as not being effective inhibitors of calcite growth due to such a small quantity. At low concentrations of phytate (≤1 μM), the formation of phytateCa precipitates at step edges is thermodynamically unlikely and the steps can advance in higher supersaturation solutions.50 Compared to phytate, oxalate is a dicarboxylic acid with dissociation constants of pK1 = 1.27 and pK2 = 4.27.51 Under alkaline conditions, the completely dissociated C2O42− species can complex with Ca2+ in solution, but no calcium oxalate precipitates can form on the step edges of calcite because the solution is undersaturated with respect to calcium oxalates (Tables S1 and S2). Moreover, the step kinetics of calcite after the addition of oxalate (0.1−100 μM) showed that the step velocity of the growth spirals was less influenced (Figure S8) than in the presence of phytate. Hence, there is little influence of oxalate on the incorporation process of humin into the calcite. Marzec et al.52 found that some amino acids could promote the burial of organic molecules by promoting the adsorption of organic molecules to the calcite surface. However, from our observations, there are no obvious differences for the adsorption of humin in the presence or absence of oxalate (Figures S11). Environmental Implications. These in situ observations demonstrate that humic substances can adsorb to calcite surfaces and then are buried into the calcite structure during the advancement of steps during spiral growth. Humic substances, as important sources of SOM, can react with minerals through both adsorption and occlusion, thus providing a novel understanding of how some SOM persists for millennia whereas others decompose readily. The buried occluded SOM within soil minerals exhibits a weak influence by environmental factors, prolonging the existence of SOM in soils in comparison to adsorbed SOM on minerals. Moreover, phytate and oxalate have different roles in influencing the burial process, suggesting that organic acids and organophosphates modulate the relative equilibrium of the occlusion and the stability of organic matter protected within soil minerals. Our results may provide new insights into organo− mineral interactions, resulting in the incorporation of SOM into minerals with a longer storage time to delay degradation in soils, and this will improve our understanding of carbon cycling and immobilization in soil ecological systems.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.8b06807. Solution conditions and supersaturations of two calcium oxalate phases, calcite surface growth in a supersaturated solution (σ = 0.140, pH = 8.3), particle sizes of three humic substances measured by AFM and DLS, detailed process of the cavity formation (σ = 1.196), occlusion of 8102


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(12) Mikutta, R.; Mikutta, C.; Kalbitz, K.; Scheel, T.; Kaiser, K.; Jahn, R. Biodegradation of forest floor organic matter bound to minerals via different binding mechanisms. Geochim. Cosmochim. Acta 2007, 71, 2569−2590. (13) Philippe, A.; Schaumann, G. E. Interactions of dissolved organic matter with natural and engineered inorganic colloids: A review. Environ. Sci. Technol. 2014, 48, 8946−8962. (14) Hejazi Mehrizi, M; Sarcheshmehpour, M; Ebrahimi, Z The effects of some humic substances and vermicompost on phosphorus transformation rate and forms in a calcareous soil. J. Soil Sci. Plant Nutr. 2015, 15, 249−260. (15) Sutton, R.; Sposito, G. Molecular structure in soil humic substances: The new view. Environ. Sci. Technol. 2005, 39, 9009− 9015. (16) Carter, P. W. Adsorption of amino acid-containing organic matter by calcite and quartz. Geochim. Cosmochim. Acta 1978, 42, 1239−1242. (17) Hoch, A. R.; Reddy, M. M.; Aiken, G. R. Calcite crystal growth inhibition by humic substances with emphasis on hydrophobic acids from the Florida Everglades. Geochim. Cosmochim. Acta 2000, 64, 61− 72. (18) Falini, G.; Fermani, S.; Tosi, G.; Dinelli, E. Calcium carbonate morphology and structure in the presence of seawater ions and humic acids. Cryst. Growth Des. 2009, 9, 2065−2072. (19) Dungait, J. A. J.; Hopkins, D. W.; Gregory, A. S.; Whitmore, A. P. Soil organic matter turnover is governed by accessibility not recalcitrance. Glob. Change Biol. 2012, 18, 1781−1796. (20) Hernandez-Soriano, M. C.; Dalal, R. C.; Warren, F. J.; Wang, P.; Green, K.; Tobin, M. J.; Menzies, N. W.; Kopittke, P. M. Soil organic carbon stabilization: Mapping carbon speciation from intact microaggregates. Environ. Sci. Technol. 2018, 52, 12275−12284. (21) Rae Cho, K.; Kim, Y.-Y.; Yang, P.; Cai, W.; Pan, H.; Kulak, A. N.; Lau, J. L.; Kulshreshtha, P.; Armes, S. P.; Meldrum, F. C.; De Yoreo, J. J. Direct observation of mineral−organic composite formation reveals occlusion mechanism. Nat. Commun. 2016, 7, 10187. (22) Liu, X.; Fu, J. W.; Guan, D. X.; Cao, Y.; Luo, J.; Rathinasabapathi, B.; Chen, Y. S.; Ma, L. Q. Arsenic induced phytate exudation, and promoted FeAsO4 dissolution and plant growth in Ashyperaccumulator Pteris vittata. Environ. Sci. Technol. 2016, 50, 9070−9077. (23) Turner, B. L.; Papházy, M. J.; Haygarth, P. M.; McKelvie, I. D. Inositol phosphates in the environment. Philos. Trans. R. Soc. London B Biol. Sci. 2002, 357, 449−469. (24) Jones, D. L. Organic acids in the rhizosphereA critical review. Plant Soil 1998, 205, 25−44. (25) Jones, D.L.; Dennis, P.G.; Owen, A.G.; van Hees, P.A.W. Organic acid behavior in soils − misconceptions and knowledge gaps. Plant Soil 2003, 248, 31−41. (26) Wang, L.; Putnis, C. V.; King, H. E.; Hovelmann, J.; RuizAgudo, E.; Putnis, A. Imaging organophosphate and pyrophosphate sequestration on brucite by in situ atomic force microscopy. Environ. Sci. Technol. 2017, 51, 328−336. (27) Keiluweit, M.; Bougoure, J. J.; Nico, P. S.; Pett-Ridge, J.; Weber, P. K.; Kleber, M. Mineral protection of soil carbon counteracted by root exudates. Nat. Clim. Change 2015, 5, 588−595. (28) Morse, J. W.; Arvidson, R. S. The dissolution kinetics of major sedimentary carbonate minerals. Earth-Sci. Rev. 2002, 58, 51−84. (29) Amrhein, C.; Zahow, M. F.; Suarez, D. L. Calcite supersaturation in soil suspensions. Soil Sci. 1993, 156, 163−170. (30) Pallo, F. J. P. In: Soil organic matter dynamics and sustainability of tropical agriculture, Mulongoy, K., Merckx, R., Eds.; Awiley-Sayce: Leuven, Belgium, 1993; pp 109−120. (31) Wang, L. J.; Ruiz-Agudo, E.; Putnis, C. V.; Putnis, A. Direct observations of the modification of calcite growth morphology by Li+ through selectively stabilizing an energetically unfavourable face. CrystEngComm 2011, 13, 3962−3966. (32) Ruiz-Agudo, E.; Putnis, C. V.; Wang, L. J.; Putnis, A. Specific effects of background electrolytes on the kineticsof step propagation

humic acid and fulvic acid particles, dissolution of calcite to expose the occluded humin particles, SEM of phytateCa precipitates, influence of low concentrations of phytate or oxalate on the occlusion, influence of oxalate on calcite growth, and the occlusion of humin particles (PDF)

AUTHOR INFORMATION

Corresponding Authors

*Phone/fax: +86-27-87288382. E-mail: [email protected]. *E-mail: [email protected]. ORCID

Lijun Wang: 0000-0001-7125-9480 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Natural Science Foundation of China (41471245 and 41071208 to L.J.W.), the National Key Research and Development Program of China (2018YFD0200900), the Fundamental Research Funds for the Central Universities (2662017PY061 to L.J.W.; 2662017JC020 to W.J.Z.). C.V.P. acknowledges funding through the EU seventh Framework Marie S. Curie ITNs: Minsc, CO2 react, and Flowtrans.

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