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DIVISION S-2—SOIL CHEMISTRY

Solid State ³¹Phosphorus Nuclear Magnetic Resonance of Iron-, Manganese-, and Copper-Containing Synthetic Hydroxyapatites

^a National Research Council, NASA, Ames Research Center, Moffett Field, CA 94035
^b Dep. of Soil and Crop Sciences, Texas A&M Univ., College Station, TX 77843
^c NASA Johnson Space Center, Houston, TX 77058

* Corresponding author (bsutter{at}mail.arc.nasa.gov)

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
The incorporation of micronutrients into synthetic hydroxyapatite (SHA) is proposed for slow release of these nutrients to crops in the National Aeronautics and Space Administration's (NASA's) Advanced Life Support (ALS) program for Lunar or Martian outposts. Solid state ³¹P nuclear magnetic resonance (NMR) was utilized to examine the paramagnetic effects of Fe³⁺, Mn²⁺, and Cu²⁺ to determine if they were incorporated into the SHA structure. Separate Fe³⁺, Mn²⁺, and Cu²⁺ containing SHA materials along with a transition metal free SHA (pure-SHA) were synthesized using a precipitation method. The proximity (<1 nm) of the transition metals to the ³¹P nuclei of SHA were apparent when comparing the integrated ³¹P signal intensities of the pure-SHA (87 arbitrary units g^-1) with the Fe-, Mn-, and Cu-SHA materials (37–71 arbitrary units g^-1). The lower integrated ³¹P signal intensities of the Fe-, Mn-, and Cu-SHA materials relative to the pure-SHA suggested that Fe³⁺, Mn²⁺, and Cu²⁺ were incorporated in the SHA structure. Further support for Fe³⁺, Mn²⁺, and Cu²⁺ incorporation was demonstrated by the reduced spin-lattice relaxation constants of the Fe-, Mn-, and Cu-SHA materials relative to pure-SHA . Inversion recovery spectra indicated that Fe³⁺, Mn²⁺, and Cu²⁺ were not homogeneously distributed about the ³¹P nuclei in the SHA structure. Extraction with diethylene-triamine-penta-acetic acid (DTPA) suggested that between 50 and 80% of the total starting metal concentrations were incorporated in the SHA structure. Iron-, Mn-, and Cu-containing SHA are potential slow release sources of Fe, Mn, and Cu in the ALS cropping system.

Abbreviations: ALS, Advanced Life Support • DTPA, diethylene-triamine-penta-acetic acid • IR, infrared • NASA, National Aeronautics and Space Administration • NMR, nuclear magnetic resonance • SHA, synthetic hydroxyapatite • XRD, x-ray diffraction

	INTRODUCTION

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THE NATIONAL AERONAUTICS AND SPACE ADMINISTRATION'S ALS PROGRAM is currently evaluating crop production systems for Lunar or Martian outposts. Crops grown will minimize resupply costs from Earth by providing food and recycling air and water (Averner, 1989; Allen et al., 1995). The ALS program is developing a zeoponic-based plant growth system which is composed of a slow release fertilizer that combines an ammonium (NH⁺₄) and potassium (K⁺) charged clinoptilolite (zeolite) with a nutrient containing SHA [Ca₁₀(PO₄)₆(OH)₂] (Golden and Ming, 1999; Steinberg et al., 2000). Synthetic hydroxyapatite is produced to contain plant essential nutrients (Mg, Fe, Mn, Cu, Zn, S, Cl, Mo, and B) within the SHA structure. If nutrients can be incorporated into the structure of the sparingly soluble SHA, then slow-nutrient release from SHA at rates suitable for plant growth would be expected. This would be ideal for missions expected to last >1 yr.

Past research using x-ray diffraction (XRD) and infrared (IR) spectroscopy has determined that Fe, Mn, and Cu were substituted into the SHA structure (Tripathy et al., 1989; Golden and Ming, 1999). Golden and Ming (1999) noted that the d[002] spacing of the Fe²⁺, Mn²⁺, and Cu²⁺ substituted SHA was less than the unsubstituted SHA. Substitution of Cu²⁺ into SHA caused the a and c axes of the Cu²⁺ substituted SHA to be less than the unsubstituted SHA (Tripathy et al., 1989). Tripathy et al. (1989) and Golden and Ming (1999) reported the PO₄-₃ absorption wavenumber of the metal substituted SHA to be lower and higher, respectively, than the unsubstituted SHA.

This research examined a lower concentration range of transition metals (7–25 g kg^-1) in SHA than were studied by Tripathy et al. (1989)(66–512 g kg^-1) and Golden and Ming (1999)(15–50 g kg^-1). X-ray analyses of the transition metal containing SHA (metal-SHA) materials of this study did not show any x-ray lines that shifted relative to pure-SHA (Sutter, 2000). The low concentration of metals in SHA did not allow for significant shift of x-ray lines that would indicate incorporation of the metals in SHA. While IR was successful in detecting Fe and Mn incorporation into SHA, IR analyses did not indicate Cu incorporation into SHA (Sutter, 2000). The amount of Cu incorporated into SHA may have been too low for IR to detect. An analytical technique was required that could detect Fe, Mn, as well as Cu incorporation into SHA for the entire metal concentration range of this research. Solid state ³¹P NMR spectroscopy proved an excellent analytical tool in detecting the incorporation of Fe, Mn, and Cu into the metal-SHA materials.

Solid state NMR can characterize the chemical environment of ³¹P nuclei through information obtained from the spectral line shape and from the NMR relaxation parameters. When cross-polarization procedures were used, an increased number of spinning sidebands of ³¹P magic angle spinning NMR resonances occurred that indicated the existence of HPO^2-₄ in SHA and other synthetic calcium phosphates (Age et al., 1984; Roberts et al., 1991; Wu et al., 1994). However, ³¹P NMR has not been used to examine the incorporation of the paramagnetic ions, Fe³⁺, Mn²⁺, and Cu²⁺ into the SHA structure. The presence of paramagnetic species complicates the examination of spinning sidebands for information on the chemical environment of the nucleus. Paramagnetic species can also give rise to spinning sidebands due to large magnetic susceptibility broadenings (Drain, 1962; Oldfield et al., 1983; Schroeder et al., 1998) in addition to any sidebands arising from the chemical shift anisotropy of the powdered sample.

The best approach to determine if Fe³⁺, Mn²⁺, and Cu²⁺ were incorporated into SHA is to examine the effect that Fe³⁺, Mn²⁺, and Cu²⁺ have on the ³¹P relaxation parameters. Nuclear relaxation by paramagnetic species has long been known (Bloembergen, 1949). Solid state NMR has been used to illustrate that Fe³⁺ substituting for Al³⁺ in kaolinite and illite caused reductions of the ²⁷Al and ²⁹Si spin lattice relaxation time constants (T₁) relative to lower Fe³⁺–containing kaolinite and illite (Hayashi et al., 1992; Shroeder and Pruett, 1996; Roch et al., 1998). Decreases in T₁ were due to the relaxation effects of the unpaired electrons from the substituted Fe³⁺.

Spin-lattice relaxation occurs when the nuclear spin is perturbed by a radio frequency pulse and then relaxes or returns to equilibrium by interacting with its surroundings or lattice, resulting in a loss of energy (Sanders and Hunter, 1993). Spin-lattice relaxation is characterized by using a time-dependent equation of the following form:

[1]

where M_t is the magnetization at time t, M_o is the magnetization at equilibrium, t is time in seconds, T₁ is the spin-lattice time constant in seconds, and b is the exponent of the argument (Sanders and Hunter, 1993). The parameter a compensates for radio frequency inhomogeneity caused by the design of the probe, and can be estimated from the ratio of the initial magnetization and the M_o from the inversion recovery experiment. When nuclei are abundant (e.g., ¹⁹F or ³¹P) and spin-diffusion is present, relaxation follows exponential recovery (i.e., b = 1). In magnetically dilute nuclear systems (e.g., ²⁹Si or ¹³C), nuclei cannot sense each other because they are too far apart; therefore, spin-diffusion does not occur. These nuclei will typically relax very slowly unless some other relaxation mechanism is present. For example,, the presence of paramagnetic species will cause these dilute nuclei to relax much faster and will be described by a nonexponential equation with b = 0.5 (Blumberg, 1960; Hayashi et al., 1992; Hartman et al., 1994). When b 1, then T₁ is referred to as T' because T₁ is a well-known constant for exponential decay processes only (Hartman and Sherriff, 1991; Sanders and Hunter, 1993). When systems have magnetically abundant nuclear systems (e.g., ³¹P) with paramagnetic centers, spin-diffusion and paramagnetic relaxation processes occur simultaneously, and b will range between 0.5 and 1 (Rorschach, 1964; Lowe and Gade, 1967; Lowe and Tse, 1968; Lewis et al., 1993).

The distance of a paramagnetic ion from the NMR active nucleus (e.g., ³¹P) also has a role in the time required for relaxation. The farther the paramagnetic ion is away from the ³¹P nucleus the less effect it will have on relaxing the ³¹P nucleus. The relaxation rate decreases at a rate of r^-6, where r is the distance of the paramagnetic ion from the nucleus. If the distance between the ³¹P and paramagnetic ion is doubled, then the relaxation rate will decrease by a factor of 64 (Sanders and Hunter, 1993). If the nucleus is too close to the paramagnetic species, then relaxation is so rapid that no signal is observed due to severe line broadening and frequency shift (Blumberg, 1960; Shroeder and Pruett, 1996). This has been described as the "wipeout sphere" model, where Fe³⁺ substituted on a regularly ordered basis for Al in kaolinite and eliminated any ²⁷Al NMR signal within a given radius of Fe³⁺ (Schroeder and Pruett, 1996). The loss of signal due to nuclei (<1 nm) close to the paramagnetic species has the effect of reducing the overall integrated signal intensity (Schroeder and Pruett, 1996). Therefore, if identical data acquisition conditions are used and there are no undetected species, materials without paramagnetic species will have larger integrated signal intensity than materials with paramagnetic species.

The overall goal of NASA's ALS program is to have a fundamental understanding of the incorporation of micronutrients into SHA and determine how useful SHA will be in supplying micronutrients to plants. This research produced singly incorporated transition metals to begin the process of examining micronutrient incorporation into SHA. The objective of this research was to utilize solid state ³¹P NMR to determine if Fe³⁺, Mn²⁺, and Cu²⁺ were incorporated into the structure of SHA. Specifically, transition metal free SHA (pure-SHA), separate transition metal phases mixed with pure-SHA, and Fe³⁺–, Mn²⁺–, and Cu²⁺–containing SHA will all be compared on the basis of (i) their integrated intensities of the ³¹P signal, (ii) spectral characteristics, and (iii) their spin-lattice relaxation (T₁ and T') behavior.

	MATERIALS AND METHODS

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Pure-SHA was synthesized by a procedure similar to Golden and Ming (1999). Calcium nitrate [Ca(NO₃)₂·H₂O] (235 g) was dissolved in 420 mL of 20% (v/v) NH₄OH while (NH₄)₂HPO₄ (72.2 g) was dissolved in 380 mL of deionized water. After the (NH₄)₂HPO₄ was completely dissolved, 30 mL of 20% (v/v) NH₄OH was added. The P solution was combined with the Ca solution and mixed by a propeller stirrer for 24 h. After mixing, the precipitate was allowed to age for 48 h. Subsequently, the NH₄OH solution was decanted and 2.5 L of deionized water was added. The SHA precipitate was mixed in water to dilute the NH₄OH and NO^-₃ and then allowed to settle. The solution was then decanted. The washing procedure to remove excess NH₄OH and NO^-₃ was repeated three more times. After washing, the apatite precipitate was separated from solution by filtering through a Whatman no. 41 filter paper. The pure-SHA precipitate was then put into an oven and heated at 400 °C for 24 h.

The transition metals were incorporated into SHA by dissolving the amounts of the transition metal materials listed in Table 1 in 100 mL of deionized water. The lowest Fe addition was based on the Fe addition used by Golden and Ming (1999) in synthesizing nutrient-substituted carbonate hydroxyapatite. Similar levels of Mn and Cu were used so the NMR analyses could compare all three metal contents. Higher Fe, Mn, and Cu additions were used to examine how T' would change with increased metal concentration. The metal solution was then added to the P solution and mixed for 5 min. The metal/P solution was then added to the Ca solution, and the remaining procedure was followed as outlined above. A total of six transition metal containing SHA (Table 1) and one pure-SHA were synthesized. When referring to the six transition metal containing SHA collectively, they will be termed metal-SHA. Numbers associated with the metal-SHA labels are their approximate concentration (g kg^-1) in SHA. All SHA materials were ground to pass through a 45-µm sieve. Iron(III) dominated in Fe-SHA on the basis of the yellow coloration of these materials and electron paramagnetic resonance spectroscopy analyses (Sutter, 2000). Manganese(II) prevailed in the Mn-SHA materials due to their pink coloring.

Diethylene-triamine-penta-acetic acid complexes with soluble and exchangeable Fe, Mn, and Cu, as well as mobilize these metals from Fe-, Mn-, and Cu-containing solid phases [e.g., metal-oxyhydroxides] (Loeppert and Inskeep, 1996). Each metal-SHA was treated with a DTPA solution to determine if the nonstructural transition metal phases detected by electron paramagnetic resonance analyses (Sutter, 2000) could affect the ³¹P spectra or the ³¹P relaxation rate. The Fe12-, Fe25-, Mn11-, Mn24-, Cu12-, and Cu20-SHA materials (0.1 g) were exposed to 35 mL of 0.001 M DTPA for 2 h on a reciprocating shaker. Subsequently, the SHA materials were centrifuged at 1271 G for 3 min and the solution decanted and filtered though 0.2-mm filter paper. Iron, Mn, and Cu solution concentrations were determined with a Perkin Elmer 3100 flame atomic absorption spectrometer (Norwalk, CT). The SHA materials were washed by adding 35 mL of deinoized water and shaken for 10 min followed by centrifugation; the washing process was repeated one more time. The SHA samples were air dried at 65 °C and then examined by ³¹P NMR. For another set of samples the above process was repeated, therefore exposing the SHA materials to DTPA for a total of 4 h. Total Fe, Mn, and Cu in the extracting solution was subtracted from starting concentration of Fe, Mn, and Cu in the metal-SHA materials to determine remaining Fe, Mn, and Cu concentrations in the metal-SHA materials.

Magic angle spinning solid state ³¹P NMR was performed on a Fourier transform Bruker (Billerica, MA) MSL 300 NMR spectrometer at room temperature (297 K). The ³¹P signal at 121 MHz was referenced to 85% (v/v) phosphoric acid (H₃PO₄). Qualitative ³¹P spectra were obtained (spin frequency 2.0 kHz) for all SHA materials to assess the spinning sideband character of the SHA spectra. Quantitative (integrated intensities) ³¹P NMR data (spin rate 4.55 kHz) were acquired for the pure-, Fe12-, Mn11-, and Cu12-SHA materials. One percent by weight of ferrihydrite (two line, 5Fe₂O₃·9H₂O) MnSO₄·H₂O, MgSO₄, and Cu(NO₃)₂·2.5H₂O were separately mixed with pure-SHA to determine the effect of these separate phases on the integrated intensity of the ³¹P signal relative to the pure-, Fe12-, Mn11-, and Cu12-SHA materials. The mixed phases were produced to simulate the occurrence of metal phases that might have precipitated separately from the metal-SHA materials. The ferrihydrite, MnSO₄·H₂O, MgSO₄, and Cu(NO₃)₂·2.5H₂O phases mixed with pure-SHA were labeled as Fe-mix, Mn-mix, Mg-mix, and Cu-mix, respectively. The qualitative and quantitative ³¹P spectra (including all observed sidebands) were acquired with a /2 excitation pulse with 5 x T₁ between scans. Acquisition time was 80 ms for each scan. Sample size was 300 mg. Sixteen scans were used for the pure-SHA and mixed phases. The Fe-, Mn-, and Cu-SHA materials had a lower signal:noise ratio than pure-SHA and therefore required 64 scans.

Inversion recovery experiments were performed using a standard –au–/2 radio frequency pulse sequence (/2 pulse width was 4 µs), where au is the time (s) of variable delay to determine T₁ or T' of all SHA and mixed pure-SHA materials. Samples were spun at a frequency of 4.55 kHz. Nonlinear least-squares analysis was used to fit the exponential (T₁ and b = 1) and nonexponential (T'and b 1) equations (Eq. [1]) to the plots of magnetization vs. the time between the and /2 pulse (variable delay) (Jandel Scientific, 1994). The T₁ or T' values were allowed to vary while the b values were manually varied until the best fit was obtained. The M_o and a values were fixed.

	RESULTS

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Total Chemical Analysis and X-Ray Diffraction
The detected amounts of Fe, Mn, and Cu in their respective SHA materials are in Table 1. X-ray diffraction plots of pure-SHA and Mn11-SHA have (hkl) reflections characteristic of apatite (Fig. 1) . The Mn24-, Fe12-, Fe25-, Cu12-, and Cu20-SHA XRD patterns (not shown) also possessed the characteristic (hkl) reflections of apatite. The Mn11-SHA along with the other metal-SHA materials exhibited increased peak broadening relative to pure-SHA. Increased strain and decreased particle size of the metal-SHA materials relative to pure-SHA caused the XRD peak broadening observed with the metal-SHA materials (Sutter, 2000).

View larger version (23K): [in this window] [in a new window]   Fig. 1. X-ray diffraction patterns of pure-synthetic hydroxyaptite (SHA) and Mn11-SHA with the primary SHA diffraction peaks (hkl) labeled.

View larger version (38K): [in this window] [in a new window]   Fig. 2. 31Phosphorus NMR spectra (2.0 kHz spin frequency) of: (a) pure-, Cu12-, Cu20-, Fe12-, Fe25-, Mn11-, and Mn24-synthetic hydroxyapatite (SHA); and (b) pure-SHA and pure-SHA mixed with 1.0 wt.% of MnSO4·H2O (Mn-mix), ferrihydrite (5Fe2O3·9H2O) (Fe-mix), Cu(NO3)2·2.5H2O (Cu-mix), and MgSO4 (Mg-mix). Spectral intensities were scaled for ease of comparison.

View larger version (33K): [in this window] [in a new window]   Fig. 3. Inversion recovery stacked 31P spectra of: (a) pure-SHA and; (b) Mn11-SHA. Arrows indicate spectra closest to zero magnetization.

View larger version (30K): [in this window] [in a new window]   Fig. 4. 31Phosphorus NMR signals passing through zero magnetization of pure-, Cu12-, Cu20-, Fe12-, Fe25-, Mn11- and Mn24-SHA after being treated 4 h with DTPA.

View larger version (59K): [in this window] [in a new window]   Fig. 5. 31Phosphorus magnetization recovery curves as a function of time for: (a) pure synthetic hydroxyapatite (SHA) and the mixture of MnSO4·H2O and pure-SHA (Mn-mix); (b) all the Metal-synthetic hydroxyapatites; and (c) Fe12-, Mn11-, and Cu12-SHA after being treated 4 h with DTPA.

[2]

where plotting

vs. t should yield a straight line when spin-diffusion is the dominant process controlling spin-lattice relaxation. A plot of

vs. t for pure-SHA was linear (Fig. 6a) . The Fe12-SHA plot was linear at longer times (>0.2 s) and then deviated from linearity at shorter times (0–0.2 s) (Fig. 6b). For the Fe12-SHA plot, an exponential equation was used (b = 1) to demonstrate that the equation did not fit at shorter times for SHA containing paramagnetic species (Fig. 6b). The lack of fit at the shorter times for the metal-SHA was the reason the nonexponential equation had a better fit than the exponential equation.

View larger version (10K): [in this window] [in a new window]   Fig. 6. The linearized form of the spin-lattice relaxation equation as a function of time for: (a) pure-SHA and (b) Fe12-SHA. The solid line indicated where spin-diffusion was controlling 31P relaxation in pure-SHA and Fe12-SHA. Points that deviated from the solid line at early times in Fe12-SHA indicated where paramagnetic effects from Fe3+ were controlling 31P relaxation.

	DISCUSSION

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Two factors together or separately can cause lower integrated intensities of the metal-SHA. The first is paramagnetic ions (Fe³⁺, Mn²⁺, and Cu²⁺) incorporated into the SHA structure enhanced the relaxation of ³¹P. The paramagnetic ions that were close (<1 nm) enough to the ³¹P nuclei completely eliminated the ³¹P signal, which contributed to a reduction in the integrated intensity (Schroeder and Pruett, 1996). The paramagnetic ions that were >1 nm from the ³¹P nuclei reduced but did not eliminate the ³¹P signal. The effect the paramagnetic ions have on the ³¹P integrated intensity decreases as the distance from the ³¹P nuclei increases (Sanders and Hunter, 1993; Schroeder and Pruett, 1996). The second factor is poorly crystalline metal phosphate that is associated with SHA. Poorly crystalline metal phases associated with SHA were detected by electron paramagnetic resonance spectroscopy and were likely to be poorly crystalline metal phosphate (Sutter, 2000). The abundance and closeness of paramagnetic ions to ³¹P nuclei in the poorly crystalline metal phosphate did not allow for a ³¹P signal to come from the poorly crystalline metal phosphate, thus causing overall lower integrated intensities in the metal-SHA/metal phosphate system (Blumberg, 1960; Hinedi et al., 1989; Shroeder and Pruett, 1996). The metal-mixed phases indicated that separate nonphosphate phases could not affect the integrated intensity of metal-SHA. The Fe-mix, Mn-mix, and Cu-mix materials did not affect the integrated intensity of the ³¹P signal because Fe³⁺, Mn²⁺, and Cu²⁺ were too far away (i.e., r^-6 dependence on relaxation) from any ³¹P nucleus to enhance relaxation. The increased distance in the mixtures indicated that Fe³⁺, Mn²⁺, and Cu²⁺ were not part of the SHA structure.

The occurrence of shoulders on the central peak of the metal-SHA materials indicated the presence of two central peaks recovering at different rates. The combination of a faster recovering peak with a slower recovering peak caused the appearance of the shoulders on the overall central peak. The faster recovering peak is indicated by the shoulders that pass through zero magnetization before the slower recovering peak. The spinning sidebands that recovered before the two central peaks were associated with the faster recovering central peak. The existence of the two peaks could be described by two T' values which indicated the existence of two phosphorus environments relaxing at slightly different rates. One possibility is a heterogeneous concentration effect where one T' was due to higher local concentrations of paramagnetic ions near ³¹P, while the other T' was due to a lower concentration of paramagnetic ions near ³¹P. The occurrence of higher and lower concentrations of paramagnetics near ³¹P would produce lower and higher T' values, respectively. Only one overall T' was determined for the metal-SHA because the difference between the two T' values was shown to be small by the observation only near zero magnetization. Poorly crystalline metal phosphate was proposed to cause the second peak. However, a second peak caused by a metal-phosphate phase is not possible because the abundance and closeness of paramagnetic species to the ³¹P nuclei in a metal-phosphate is too great to allow for an observable ³¹P signal (Blumberg, 1960; Hinedi et al., 1989; Schroeder and Pruett, 1996). This was proven with FePO₄·H₂O which did not yield a ³¹P signal (data not shown). Hinedi et al. (1989) also did not obtain a ³¹P NMR spectra of Fe- and Mn-phosphate minerals because of strong paramagnetic effects.

The rapid magnetization recoveries of the metal-SHA and the metal-SHA treated with DTPA when compared with the pure-SHA indicated that the metals in those samples were incorporated close (<1 nm) to the ³¹P nucleus, and must be part of the SHA structure. The Fe-mix, Mn-mix, and Cu-mix magnetization recoveries were similar to the pure-SHA recoveries, indicating that the separate metals phases in the metal-SHA could not be responsible for rapid magnetization recoveries observed in the metal-SHA samples. The rapid magnetization recovery of the metal-SHA materials also indicates that Fe, Mn, and Cu incorporated into the SHA structure were at least partly responsible for the reduced integrated signal intensity.

The metal-SHA data were best described with a nonexponential equation (b = 0.69–0.79). If b was to equal 0.5 for the metal-SHA, then ³¹P relaxation would be due solely to paramagnetic effects (i.e., no spin diffusion). The range of b values between 0.69 to 0.79 indicated that both spin diffusion and paramagnetic effects were responsible for ³¹P relaxation in the metal-SHA materials (Rorschach, 1964; Lowe and Gade, 1967; Lowe and Tse, 1968; Lewis et al., 1993). Spin diffusion was expected in all SHA materials because ³¹P is a magnetically abundant species. Paramagnetic relaxation of ³¹P nuclei would be expected if the paramagnetic ions (Fe³⁺, Mn²⁺, and Cu²⁺) were incorporated into the SHA structure and near the ³¹P nuclei on the order of 1 nm.

The lower T' values of the metal-SHA and the metal-SHA treated with DTPA relative to the T₁ of pure-SHA indicated that Fe³⁺, Mn²⁺, and Cu²⁺ were effective at reducing the relaxation time of ³¹P. The reduced relaxation time provided further support that Fe³⁺, Mn²⁺, and Cu²⁺ were incorporated into the SHA structure and were within atomic scale distances of the ³¹P nuclei.

As the concentration of the metals increased, the T' values decreased, indicating a T' dependence on metal concentration. The higher metal concentration caused more metals to interact closely with the P nuclei. This led to increased paramagnetic relaxation effects on the P nuclei, resulting in lower T' values.

The higher T₁ reported for pure-SHA with DTPA treatment was attributed to removal of paramagnetic impurities that were acquired from the reagents used to synthesize pure-SHA. No impurity effect would have been observed in the metal-SHA because the added paramagnetic ions dominated the relaxation process. The DTPA treatment was performed to see if any Fe³⁺, Mn²⁺, and Cu²⁺ were removed from SHA that might have affected the relaxation of the ³¹P signal. The trend of increasing T' with DTPA treatment for the Mn- and Cu-SHA materials indicated that the DTPA removed Mn²⁺ and Cu²⁺ from the SHA structure, causing a reduction in the amount of Mn²⁺ and Cu²⁺ interacting with P. The reduction in the Mn²⁺ and Cu²⁺ concentration of SHA was confirmed by the concentrations of Mn²⁺ and Cu²⁺ being lower in SHA treated by DTPA than SHA not treated by DTPA (Table 1). Lower concentrations of Mn²⁺ and Cu²⁺ in the SHA decreased the paramagnetic relaxing effects on the P nuclei, causing T' to increase. While DTPA extracted structural metals from SHA, the removal of poorly crystalline metal phases associated with SHA also contributed to the decrease in the total starting metal concentrations. The difference between the 2- and 4-h DTPA extractions are not large, indicating that DTPA could not remove significantly more metal from SHA. The metals remaining after a 4-h treatment were metals strongly incorporated into the SHA structure. Examination of the 4-h DTPA metal concentration data suggests that between 50 and 80% of the total metals before DTPA extraction were incorporated into the SHA structure. Unlike the Mn- and Cu-SHA materials, T' for the Fe-SHA materials did not change significantly with DTPA treatment, despite the reduction of Fe concentration (Table 1). A possible explanation was that DTPA only extracted Fe not closely associated with P, and did not extract structural Fe that was closely associated with P. Nevertheless, T' values remained extremely low after all DTPA treatments for the metal-SHA, indicating that the transition metals were within the SHA structure and inaccessible to DTPA.

The linear plot of the exponential equation (b = 1) for pure-SHA was a near-perfect fit and supports the presence of spin diffusion throughout the entire relaxation period. The fit for the same linear exponential plot for Fe12-SHA fits the data well at times >0.2 s because spin-diffusion was the dominant relaxation process at the longer times. The linear exponential line deviated from linearity at times <0.2 s, indicating that direct dipolar coupling with the electron spin of the paramagnetic species was responsible for ³¹P relaxation at the times <0.2 s (Hayashi et al., 1992). Paramagnetic relaxation was extremely rapid, and dominated at an early stage of the relaxation process (Blumberg, 1960).

	CONCLUSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
The two processes that affected ³¹P relaxation in the metal-SHA materials were spin-diffusion and paramagnetic effects. Spin-diffusion was due to the abundance of ³¹P nuclei while the paramagnetic effects were due to the incorporation of Fe³⁺, Mn²⁺, and Cu²⁺ into SHA. The presence of paramagnetic impurities rendered the extraction of chemical bonding information difficult due to the problem of separating chemical shift anisotropy effects from magnetic susceptibility broadening. Hence, spin-lattice relaxation proved to be a better approach for showing that Fe³⁺, Mn²⁺, and Cu²⁺ were incorporated into the SHA structure. The range of b (0.63–0.79) for the metal-SHA materials supported the presence of spin-diffusion and paramagnetically controlled relaxation. The exponential fit at times >0.2 s in the metal-SHA supported the existence of spin-diffusion effects on ³¹P relaxation. The low T' values, decreased integrated intensities of the ³¹P spectra, and the lack of exponential fit at times <0.2 s supported paramagnetic effects on ³¹P relaxation. The significantly lower integrated intensities of the ³¹P NMR spectra and lower T' values of the metal-SHA relative to the pure-SHA indicated that Fe³⁺, Mn²⁺, and Cu²⁺ ions occurred near the ³¹P nuclei on the order of 1 nm and were incorporated into the SHA structure.

Nuclear magnetic resonance spectroscopy cannot unequivocally prove that the Fe³⁺, Mn²⁺, and Cu²⁺ substituted for Ca²⁺ in the SHA. Nevertheless, the enhanced relaxation of the ³¹P nuclei in metal-SHA indicated that Fe³⁺, Mn²⁺ and Cu²⁺ were close to P on an atomic scale. The closeness of Fe³⁺, Mn²⁺ and Cu²⁺ to P indicated bonding with phosphate, suggesting substitution of these transition metals into one or both of the Ca sites. The metal-substituted SHA materials will act as slow-release fertilizers of Fe, Cu, Mn, Ca, and P. The SHA materials could be used as a slow-release source of these elements in solid substrates used in the ALS cropping system, as well as terrestrial agriculture applications.

	ACKNOWLEDGMENTS

 
This research was partially funded by NASA's Graduate Student Researchers Program (NGT 51229) in conjunction with Johnson Space Center, Houston, TX. The authors would like to thank Ray Guillemette for his assistance with electron microprobe analyses. The authors are grateful to Dr. Richard Morris, the three anonymous reviewers, and the associate editor Dr. Cliff Johnston for their critical review of this manuscript.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 

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