FTIR, XAS, and XRD study of cadmium complexes with l -cysteine

Polyhedron 56 (2013) 237–242

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FTIR, XAS, and XRD study of cadmium complexes with L-cysteine Jason G. Parsons c,⇑, Kenneth M. Dokken a, John McClure b, Jorge L. Gardea-Torresdey a a

Department of Chemistry, University of Texas at El Paso500 W. University Ave., El Paso, TX 79968, United States Department of Metallurgical and Materials Engineering, University of Texas at El Paso500 W. University, El Paso, TX 79968, United States c Department of Chemistry, University of Texas-Pan American 1201 W University Dr., Edinburg, TX 78539, United States b

a r t i c l e

i n f o

Article history: Received 6 February 2013 Accepted 1 April 2013 Available online 8 April 2013 Keywords: Cadmium(II) L-cysteine complexes XAS Phytochelatin model compound Metallothionine model system

a b s t r a c t Cysteine (cys) plays a vital role in the detoxification of cadmium (Cd), but the coordination of this metal to cys is not well understood, although extensively studied. In this investigation, our results showed that the ratio Cd:cys 1:2 precipitate as a amorphous white powder, the Cd:cys 1:4 provided for a viscous liquid without precipitating, while the Cd:cys 1:6 resulted in long, clear, needle-like crystals. FTIR and XAS analysis indicated that cys was coordinated to Cd through S ligands on the cys. EXAFS of the Cd:cys products showed small differences in the coordination environment. The complex from Cd:cys 1:2 reaction displayed two different Cd–S interactions at 2.69 and 2.54 Å, each consisting of two neighboring atoms. The complex from the Cd:cys 1:4 reaction showed four equally distant Cd–S interactions at 2.47 Å. The comples from the Cd:cys 1:6 reaction exhibited a Cd–S interaction of four S ligands at approximately 2.54 Å. All the Cd:cys complexes had a tetrahedral arrangement of S ligands around the central Cd atom. The XRD demonstrated that the Cd:cys 1:2 and 1:4 reaction products were amorphous and no diffraction peaks were observed. However, the Cd:cys 1:6 reaction product showed strong diffraction peaks, crystallizing into a monoclinic unit cell (C2/C). Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction Cysteine (cys) plays a vital role in the synthesis of peptides and proteins and in the detoxification of heavy metals such as cadmium and mercury in living organisms [1–4]. Plants are known to synthesize phytochelatins as well as metallothionine, which are cysteine rich compounds that coordinate to heavy metals for storage and detoxification [1–4]. Phytochelatins are known to have the following general sequence [-c-glu-cys]n-gly, where n can be up to 11 [5]. However, other living organisms such as yeasts, humans, and mammals (among others) have been shown to synthesize metallothioneins, which are cysteine rich compounds structurally related to phytochelatins that effectively bind heavy metals for storage, detoxification, and/or excretion [6]. Metallothioneins, expressed in mammals, have been structurally determined to contain between 60 and 62 amino acid residues of which 18 to 20 are cysteine residues [6]. The active sites in both phytochelatins and metallothionines have been investigated using a number of models including coordination compounds consisting of cadmium, zinc, or mercury and low molecular weight thiols such as methanthiol and ethanedithiol [6,7]. Phytochelatins and metallothionines systems have also been studied using cadmium phenylthiol ([Cd(SPh)4]2, [Cd2(l-SPh)2

⇑ Corresponding author. Tel.: +1 (956)381 7462; fax: +1 (956)384 5006. E-mail address: [email protected] (J.G. Parsons). 0277-5387/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.poly.2013.04.001

(SPh)6]2, and [Cd4(l-SPh)6(SPh)4]2 complexes to determine the active site for metal binding [1,6,5,8]. These studies have determined that the coordination in both the metallothionein and phytochelatin systems consists of a cage-like structure in which the cadmium ions are tetrahedrally coordinated to sulfur ligands. In a study of Cd complexes with glycine, L-alanine, and L-cys the structure of Cd(cys)4 could not be determined due to the formation of a viscous liquid [9]. The authors suggested that the complex was similar to that of the glycine, and L-alanine Cd complexes. NMR studies also suggested the presence of cadmium-oxygen bonds from the carboxyl groups on the cys in the complex [9]. However, the presence of an oxygen ligand has not been reported in the literature pertaining to the metallothionein or phytochelatin complexes of heavy metals. The absence of metal oxygen bonds in both phytochelatin and metallothionein complexes, as well as in the models used to describe these systems could be an artifact of the number of oxygen ligands in the model and actual systems. For example, a very low number of Cd–O bonds would not be very visible in a system with a much high number of Cd–S bonds. In addition, the model compounds ([Cd(SPh)4]2, [Cd2(l-SPh)2 (SPh)6]2, and [Cd4(l-SPh)6(SPh)4]2) used to determine the active site in phytochelatins and metallothionines do not have oxygen ligands present in the structure for binding [1,6,5,8]. However, recently through supplication of chemical structural techniques Jalelihvand et al have investigated the interactions of cadmium with cysteine and Penicillamine, which showed mixed coordination environments consisting of Cd–S and Cd–O(N) at distances

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of approximately 2.54 and 2.28–2.33 Å, respectively [10]. In addition, Jalelihvand et al have also investigated the coordination environment of cadmium(II) cysteine complexes in the solid state, which potentially showed a mixed coordination environment for cadmium(II) cysteinates with the following molecular formulas: Cd(Hcys)2 H2O and {Cd(Hcys)2 H2O}2 H3O+ClO4. This manuscript showed that the cadmium is coordinated to both the sulfur and nitrogen or oxygen ligand at interatomic distances of 2.52 and 2.27 Å, respectively [11]. In the present study, the synthesis and structural determination of cadmium(II) cys complexes was performed was performed at three different molar ratios. The Cd:cys complexes were synthesized in anhydrous methanol, at molar ratios of 1:2, 1:4, and 1:6 (cadmium: cysteine). The resulting compounds were studied using a combination of FTIR, XAS, and XRD to determine the structural characteristics in terms of the binding modes of Cd to the cysteine, the coordination environment, and the crystal lattice of the complexes. 2. Methodology 2.1. Synthesis of cadmium cysteine complexes Cd–cys complexes were synthesized using (Cd(NO3)24H2O) (Aldrich) and L-cys hydrochloride anhydrous (Aldrich). The complexes were synthesized using mole ratios of 1:2, 1:4, and 1:6 of Cd:Cys. L-cys hydrochloride (L-cys HCl) was dissolved in 50 mL of methanol and then Cd(NO3)2 was added to the mixture. The mixtures were stirred on a hot plate over low heat. After several minutes of reaction a white powder precipitated, a viscous liquid formed, and long needle-like crystals formed for the 1:2, 1:4, and 1:6 reactions, respectively. Once the different products were formed, they were removed from the hot plate. The samples were stored in micro-centrifuge tubes, in the dark, until analysis. 2.2. IR spectroscopy Infrared spectra of the compounds were collected using 2% by weight KBr pellets of the complexes. The spectra were collected using a Perkin Elmer Spectrum 100 FTIR spectrometer (Perkin Elmer Inc., Waltham, MA). To improve signal to noise ratios, 32 scans of each sample were collected and co-added at a resolution of 2 cm1. The background was determined using a pure KBr pellet using the same parameters as the samples. The final spectra were baseline corrected and normalized to one absorption unit.

2.4. XAS data reduction The sample spectra and the model compound (cadmium sulfide) were analyzed using the WinXAS software (V 3.1) and standard data reduction techniques [12,13]. The data were first energy calibrated using the second degree derivative of the internal Cd(0) reference (E0 = 26.711 keV). The sample spectra were then background corrected using a 1st degree polynomial fitting on the pre-edge region and a 4th degree polynomial fitting on the post edge region. Subsequent to background correction, the sample spectra were normalized to 1 absorption unit. After normalization, the XANES spectra were extracted from 26.700 keV through 26.850 keV. The EXAFS were then extracted from the background corrected normalized spectra using the procedure outlined below: The sample spectra were converted into k-space (or wave-number space Å1) based on the energy of the photoelectron ejected from the sample. The conversion into k-space was performed by taking a second degree derivative of the energy-corrected sample spectra, which was determined to be the E0 of the sample. After conversion into k-space the spectra were l fitted using a spline of 4 knots and a k-weight of 3. The spectra were then Fourier transformed from 2.0 to 12.2 Å1, into R-space (Å). The sample spectra were then subsequently back transformed into k-space from 1.0 to 2.6 Å, to extract the first coordination shell EXAFS. The back transformed EXAFS spectra were fitted to determine the coordination numbers (CN), interatomic distances (R), Debye-Waller factors, and the S02 factors, using linear least squared fittings of calculations from FEFF V 8.00 [14]. The inputs for the FEFF calculations were generated using the ATOMS software V 3.0 beta and crystallographic data for cadmium sulfide from the literature [15,16]. 2.5. XRD data collection The powder sample was ground into a fine powder using a mortar and pestle to obtain a homogenous mixture and then fixed onto a microscope slide using acetone. The liquid sample was viscous and sticky and adhered by itself to the microscope slide. The diffraction patterns for the samples were then collected using a Sintag XDS 2000 X-ray diffractometer (Thermo Fisher Scientific, Madison, WI) with a copper source (k = 1.541 Å). The samples were collected using a h2h geometry with a counting time of 0.5 s and a step of 0.02°. The diffraction patterns were then background corrected and normalized and fitted using WINFIT (Novocontrol Technologies, Hundsangen, Germany) and the cell parameters and unit cell were determined using the CHEKCELL software [17].

2.3. XAS data collection 3. Results and discussion XAS Spectra were collected on beamline 10-2 at Stanford Synchrotron Radiation Lightsource (SSRL, Palo Alto, CA) using standard conditions at the cadmium K-edge (E0 = 26.711 keV). The sample spectra were collected at room temperature using the following conditions: a current ranging between 80 and 100 mA, beam energy of 3.0 GeV, a Si 220 (u 90) double crystal monochromator, a 1.0 mm by 10.0 mm up-stream slit, and argon filled ion chambers. The samples were collected in transmission mode using an internal Cd(0) metal foil (E0 = 26.711 keV) for calibration purposes. In addition, the beam was detuned by 30% to reduce higher order harmonics (to aid in data analysis). The samples and model compounds were diluted to 5% by mass using boron nitride, which was performed by homogenizing the samples by weighing a specific amount of boron nitride and grinding with a specific mass of the compound in a mortar and pestle. The samples were then packed into 1 mm Al sample holders with KaptonÒ tape windows for XAS analysis.

The FTIR spectra collected for each of the synthesized compounds and the starting material L-cysteine hydrochloride (L-cysHCl) are shown in Fig. 1. The peak assignments are shown in Table 1. The spectra collected for each of the Cd(II):cys are almost identical, but show some significant structural differences from the parent compound L-cysteine-HCl. The first observable difference in the spectra) is the sulfur–hydrogen (S–H) stretching observed at 2558 cm1 in the L-cysHCl compound, shifted by approximately 20 to 2538 cm1. In addition, this stretch becomes less intense and more diffuse, which may indicate that there are still some S–H stretches are present in the compounds. Similarly, the S–H stretch at 988 cm1 in the L-cys-HCl is still present in the synthesized Cd:cys compounds, but the intensity of the stretch has been dramatically reduced indicating that there are still some free S–H groups present in the Cd–cys complexes. Other notable changes in the IR spectra of the Cd:cys

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3.5

Cd:Cys 1:6

2.5

Cd:Cys 1:4

2

1.5

Cd:Cys 1:2 1

L-Cys HCl 0.5

0 4000

3500

3000

2500

2000

1500

1000

500

-1

Wavenumber (cm ) Fig. 1. FTIR of L-cysteine hydrochloride and the reaction products of 1 mole of cadmium(II) nitrate tetrahydrate with 2, 4, and 6 moles of L-cysteine hydrochloride.

Table 1 Infrared band assignment of L-cysteine hydrochloride and cadmium(II) cysteine complexes in mole ratios of Cd:Cys of 1:2, 1:4, and 1:6. L-Cys

HCl

Cd:Cys 1:2

Cd:Cys 1:4

Cd:Cys 1:6

Assignment

3434 m, br

3461 m, br

3443 m, br

3115 3078 3013 2919 2851

3116 3078 3011 2944

3115 3078 3009 2945

v v v v v v v v v v

3394 sh

2989 sh

2641 w 2607 w 2558 m 2507 m 1741vs 1642 w 1619 w 1569 mw 1519 vs 1425 m 1396 m 1344 w 1313 w 1270 w 1219 vs 1139 mw 1105 mw 1056 mw 988 w 928 w 867 mw 836 w 798 w 774 w 736 w 678 w 640 mw 607 w 523 w

vs sh s vs sh

vs sh s sh

vs sh s sh

2538 mw

2540 mw

2542 mw

1739 vs

1742 vs

1742 vs

1586 mw 1486 vs

1586 mw 1491 vs

1586 mw 1493 vs

1384 1358 1325 1251 1212 1121 1093 1057

1384 1364 1325 1248 1203 1128 1093 1059

sh mw w mw w mw w m

sh mw w m vs m w m

921 w 846 w 833 m

926 w 846 mw 833 m

1384 m 1363 mw 1325 w 1248 m 1203 s 1131 m 1093 w 1060 m 991 w 927 w 846 mw 833 m

785 w

782 w

782 w

676 w

676 w

676 w

598 w 529 w

598 w 521 w

598 w 523 w

OH (H2O) OH (H2O) NH2 NH3 CH2, v CH3 NH3+, v CH2, v CH3 CH2, v CH3 CH2 CH2 SH

v d d d

CO NH3+ NH3+, v as COO NH3+, v as COO c NH3+ d as CH3, d as CH2 vs COO vs COO00 , d OH(COOH) w CH2 c CH2 v CO, d OH (COOH) NH3+ v CN, v CC D SH v CN, v CC v CC, d COO d COO r CH2 c CH2 v CS d COO v CS

c COO

4.0 Normalized Absorption

Normalized Absorption

3

complexes and the L-cysHCl compound are that the C–S (736 and 640 cm1) stretches in the L-cysHCl are missing in the Cd:cys complexes. The disappearance of the C–S bond vibrations are indicative of S being bound to a heavy element such as Cd. The loss of these stretches was reported in a paper by Dokken et al. [16] who studied Cu–cys complexes [18]. The FTIR data indicates that the coordination of Cd to the cysteine occurs through the S ligand present on the cys. In addition, the fact that the other potential binding groups on the cys ligand (COOH and NH2) are unaffected to any substantial amount after the coordination indicates that the binding is occurring for the most part through the S group. The shifting observed in the COOH and the NH2 groups on the Cd:cys complexes compared to the model compound are possibly due to the formation of hydrogen bonds between the COOH and the nitrogen atom on the NH2 group. The formation of the hydrogen bond between the COOH and the NH2 group on the cysteine would cause approximately a 20 cm1 shifting without eliminating the stretches, which is observed in the data. The only IR stretches affected dramatically by the ligation of Cd are the S–H and the C–S indicating that these groups are involved directly in the Cd coordination. The cadmium K-edge XANES spectra for the Cd:cys complexes at different cys ratios and the Cd sulfide model compound are shown in Fig. 2. The Cd:cys complexes have the same inflection point in the edge as the Cd sulfide model compound, indicating that the binding in the Cd:cys complexes is through the S ligands. The presence of oxygen or nitrogen ligands in the system should cause an energy shift or the appearance of a shoulder in the absorption edge. However, all the Cd:cys complexes and the Cd–sulfide model compound have the same inflection point in the edge as indicated by the vertical dotted line in Fig. 2. The only difference in the spectra of the Cd–cys complexes and the Cd–sulfide model compound is the feature at 26.74, which is more pronounced in the Cd:cys complexes. This change in the shape of the feature at 26.74 keV indicates a shift in the geometry from the Cd–sulfide model compound, which is tetrahedral with Cd–S at 2.52 Å and Cd–Cd interactions at 4.11 Å [19]. The EXAFS of the Cd–sulfide model compound and Cd:cys complexes are shown in Fig. 3. As can be seen in Fig. 3, there are only slight deviations in the position of the main oscillation between the Cd–sulfide and the Cd:cys complexes. The FEFF fittings of EXAFS are shown in Table 2, which also show a slight

Cd-Sulfide

Cd:6 moles Cys

3.0

Cd: 4 moles Cys

2.0

Cd: 2 moles Cys 1.0

26.75

26.8 Energy [keV]

26.85

Fig. 2. XANES region from 26.700 to 26.850 keV of the cadmium(II) sulfide model compound and the product from the reaction of 1 mole of cadmium(II) nitrate tetrahydrate with 2, 4, and 6 moles of L-cysteine hydrochloride.

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3

5

0 -2

4 -4

3 -6

2

4

6

8

10

12

-1

k[Å ]

1 0 0

1

2

3

4

5

6

7

2 1

2.5

3

2

6

B Χ(k)*k

7

Fourier Transform Magnitude

A Χ(k)*k

Fourier Transform Magnitude

8

3

4

2

0 -1 -2

1.5

-3

4

1

6

8

10

12

-1

k[Å ]

0.5 0 0

8

1

2

3

R[Å]

4

5

6

7

8

R[Å] 6

3

4

0

3 -5

2

4

6

8

10

12

-1

k[Å ]

1 0 0

1

2

3

4

5

6

7

8

4 2 3

4

Χ(k)*k

6 5

D

5

Fourier Transform Magnitude

C Χ(k)*k

Fourier Transform Magnitude

7

5

3

0 -2 -4 -6

2

-8

2

4

6

8

10

12

-1

K[Å ]

1 0 0

1

2

3

4

5

6

7

8

R[Å]

R[Å]

Fig. 3. (A) Fourier transformed EXAFS of cadmium sulfide model compound (dotted line) and Fourier transformed EXAFS of the fitting of the back transformed cadmium sulfide model compound EXAFS (solid line). (B) Fourier transformed EXAFS of cadmium(II) nitrate treated with 2 moles of L-cysteine hydrochloride (dotted line) and Fourier transformed EXAFS of the fitting of the back transformed cadmium(II) nitrate treated with 2 moles of L-cysteine hydrochloride EXAFS (solid line). (C) Fourier transformed EXAFS of cadmium(II) nitrate treated with 4 moles of L-cysteine hydrochloride (dotted line) and Fourier transformed EXAFS of the fitting of the back transformed cadmium(II) nitrate treated with 4 moles of L-cysteine hydrochloride EXAFS (solid line). (D) Fourier transformed EXAFS of cadmium(II) nitrate treated with 6 moles of L-Cysteine hydrochloride (dotted line) and Fourier transformed EXAFS of the fitting of the back transformed cadmium(II) nitrate treated with 6 moles of L-cysteine hydrochloride EXAFS (solid line). The inserts in each of the figures shows the raw EXAFS (dotted line) the back transformed EXAFS (dashed line) and the fitting of the back transformed EXAFS.

Table 2 Linear least squared fittings of cadmium cysteine EXAFS and cadmium(II) sulfide model compound EXAFS using parameters derived from FEFF V8.00. Sample

Interaction

CN

R (Å)

r2 (Å2)

S02

Cd: 2 cysteine

Cd–S Cd–S Cd–Cd Cd–S Cd–S Cd–Cd Cd–S Cd–Cd

2.0 2.0 1.0 4.0 4.2

2.55(5) 2.69(1) 3.98(4) 2.47(5) 2.54(4) 3.89(9) 2.51(5) 4.12(5)

0.0033 0.0055 0.012 0.0055 0.0096 0.012 0.0055 0.017

0.89

Cd: 4 cysteine Cd: 6 cysteine Cadmium(II) sulfide

4.0 6.0

0.91 0.93 0.95

difference between the interatomic distances between the Cd–sulfide and the Cd:cys complexes. From the fitting of the Cd sulfide model compound, it is shown that Cd ions have four S ligands attached at an interatomic distance of 2.51 Å, which indicates a tetrahedral arrangement of S ligands around the central Cd ion (Fig. 3A). In Cd, (treated with two mole equivalents of L-cys hydrochloride) the fittings of the EXAFS data indicate that there are two different types of S binding to the central Cd ions (Fig. 3B). The EXAFS fittings show that there are two S ligands at approximately 2.69 Å and two more S ligands at approximately 2.55 Å, as shown in Table 2. These two bond lengths are indicative of a complex consisting of terminal cysteine and bridging cysteine ligands; the longer bond lengths are associated with the bridging S ligands in

the cys and the shorter bond lengths are consistent with the terminal ligands [1,11]. In addition, the sample did not crystallize, it gave an amorphous sample as shown in the diffraction data in Fig. 4. A proposed structure based on the data collected from the EXAFS spectroscopy is presented in Fig. 5 A, which shows the different types of ligands present in the sample, the terminal cys which have the short binding distance of 2.55 Å, and the two bridging S ligands with the long binding distance of 2.69 Å. Similar types of structures have been shown in the literature for Cd treated with phytochealtins, cysteine, and other thiol containing ligands [1,8,20,21]. The EXAFS of the Cd ions treated with four mole equivalents of L-cys hydrochloride is shown in Fig. 3C. The fitting of this sample shows that the coordination consists of four equally spaced S ligands at a short interatomic distance of 2.47 Å. The Cd–S interatomic distance of 2.47 Å is shorter than the Cd–S interatomic distances in Cd–sulfide of 2.51 Å, as shown in Table 2. This coordination indicates that the cys arranged around the Cd are in a tetrahedral arrangement with equivalent bond lengths (i.e. there are no bridging S ligands). In addition, the sample did not precipitate or crystallize; it remains as a clear viscous liquid which has been noted in the literature with Cd coordinated with four cys molecules [9]. The proposed structure for the 1:4 Cd:cys complex is shown in Fig. 5 B. The Cd treated with six mole equivalents of L-cys hydrochloride produced a product present in two phases: a liquid phase and a crystalline phase. However, over time the 1:6 Cd:cys sample became completely crystalline. The EXAFS of the 1:6 Cd:cys product are shown in Fig. 3D and the EXAFS fittings are presented in Table 2. As can be seen from

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Normalized Intensity

1.0

A

0.8

0.6

0.4

0.2

0.0 10

15

20

25

30

2θº

Normalized Intensity

1.5

B

1.0

1 Cd: 6 Cys 0.5 1 Cd: 4 Cys 1 Cd: 2 Cys 0.0 10

15

20

25

30

2θº Fig. 4. (A) Powder X-ray diffraction pattern for L-cysteine hydrochloride starting material. (B) Powder X-ray diffraction patterns for reactions between cadmium and Cysteine at molar ratios of 1 cadmium: 2 Cysteine, 1 cadmium: 4 Cysteine, and 1 cadmium: 6 Cysteine.

the fittings the sample showed that there are approximately four Cd–S in the sample with an interatomic distance of 2.54 Å [4]. However, at further interatomic distance there are heavy backscattering elements, which are indicated in the EXAFS. For the 1:2 Cd:cys compound the fitting of the EXAFS data indicated the presence of

A

one cadmium atom at an interatomic distance of 3.98 Å. The presence of one cadmium atom at an interatomic distance of 3.98 Å has been suggested in the literature for cadmium reacting with two cysteine molecules. There was no observable Cd–Cd interaction in the 1:4 Cd:cys treatment. However, in the 1:6: Cd:cys treatment 2 Cd–Cd interaction were observed in the second shell at an interatomic distance of 3.89 Å. The 1:6 cd:cys treatment indicates the formation of a cluster type of compound. The presence of Cd–Cd interactions has been proposed by other authors in the study of Cd–phytochealtin and Cd–metallothionein complexes [1,8,20,21]. The cage type structure consists of two different Cd–Cd interatomic distances: one at a short distance and one at a much longer distance, approximately 3.84 and 4.11 Å, respectively, which average out to an interatomic distance of 3.98 Å. This type of structure is presented in Fig. 5 C, which shows only the Cd–S interactions. In phytochealtin model compounds, the Cd–S interatomic distance has been shown to range from 2.47 to 2.61 Å, with a coordination number of four, as determined through X-ray studies [1,11,12]. Similar compounds have been studied using XAS and the coordination was determined to consist of four Cd–S interactions with interatomic distances of approximately 2.54 Å [1]. In metallothionein compounds using XAS studies and density functional theory it has been shown that Cd in these types of cluster compounds can have over extended S interactions at interatomic distances of approximately 2.70 Å [8]. Unlike the work presented by Jalielhavand et al, which has shown the presence of Cd–O interactions, the present study does not show indicate the presence of a light atom such as oxygen or nitrogen at 2.28 Å [11]. Jalielhavand et al fitted the small shoulder appearing on the Cd–S EXAFS with an oxygen atom, however they noted that it only improved a minimal amount. This shoulder may be an effect of the mixing of the waver functions from the two Cd–S interactions at the different interatomic distances. Cadmium treated with thiol compounds in aqueous solution causes the coordination environment to deviate from the pure Cd–S interaction to have a mixed coordination environment which consists of S ligands and oxygen ligands at 2.52 and 2.28 Å, respectively [11,21]. It has also been shown in the literature that the maximum coordination of Cd ions with small ligands such as oxygen and nitrogen is six; however, with larger ligands such as S the coordination maximizes at four due to space limitations or steric hindrance, which limits the geometry to tetrahedral [19]. The results this manuscript reflect the different types of coordination observed in cadmium glutionine and cadmium metallothionine complexes observed in plants yeast and in mammals [22]. The formation of the cage type structure observed in the 1:6

B

C Cd-S 2.47Å

Cd-S 2.69Å Cd-S 2.55Å

Cd-S 2.54Å

Fig. 5. Proposed structures of cadmium Cysteine complexes from the reaction of 1 mole of cadmium nitrate tetrahydrate with 2 moles of L-cysteine hydrochloride (A), 1 mole of cadmium nitrate tetrahydrate with 4 moles of L-cysteine hydrochloride (B), and 1 mole of cadmium nitrate tetrahydrate with 6 moles of L-cysteine hydrochloride (C) derived from EXAFS calculations.

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Table 3 Cell parameters determined from the powder XRD patterns using the

CHECKCELL

software.

Sample

a (Å)

b (Å)

c (Å)

a (°)

b (°)

c (°)

V (A3)

Cell

L-cysteine

19.48

7.12

5.52

90

90

90

765.6

P212121

N/A N/A 14.37

N/A N/A 6.97

N/A N/A 18.03

N/A N/A 90

N/A N/A 92.27

N/A N/A 90

N/A N/A 1803

N/A N/A P21/C

HCl Cd: 2 cysteine Cd: 4 cysteine Cd: 6 cysteine

Cd:cys treatment, may be due to the reaction environment, the increased amount of chlorine in the 1:6 Cd:cys treatment may play an important role in the formation of the cage type system for the Cd with the cys molecule. The increased Cl concentration from the L-cysteine HCl, at the 1:6 Cd:cys treatment, may facilitate the formation of the cage type structure. However, this is speculative and further study need to be performed to understand this complex formation. The diffraction patterns for the L-cysteine hydrochloride starting material and the Cd–nitrate tetrahydrate treated with L-cys hydrochloride at molar ratios of 1:2, 1:4, and 1:6 Cd:cys are shown in Fig. 4A and B. As can be seen in Fig. 4 A and Table 3, the L-cys hydrochloride is a crystalline solid with a rhombohedral unit cell. The fitting of the L-cys hydrochloride crystals is in agreement with published crystal structures [23]. L-cys hydrochloride has also been shown to crystallize into a monoclinic crystal structure [24]. In the synthesized Cd:cys compounds, the 1:2 and the 1:4 complexes were amorphous showing no diffraction peaks ranging between 5° and 30° in 2h, and thus no unit cell was determined. However, the 1:6 complex showed sharp diffraction peaks in the diffracted range from 5° to 30° in 2h. From the diffraction pattern and the use of the CHEKCELL software, it was determined that the product from the 1:6 Cd:cysteine reaction crystallized into a monoclinic unit cell (C2/C) with the cell parameters listed in Table 3. The determined cell of the 1:6 Cd:cysteine reaction product agrees with the unit cells of Cd crystallizing with different thiol compounds and amino acids [9,16,25,26]. In addition, it is also shown in the literature that heavy metal–cys and cys derivative complexes commonly crystallize with either orthorhombic or monoclinic unit cells [16,27,28]. 4. Conclusions We have successfully synthesized stable Cd–cys compounds that show the coordination environment very similar to phytochelatin and metallothionein compounds from reactions using mole ratios of Cd:cys of 1:2, 1:4, and 1:6. At the highest mole ratio of (Cd:cys, 1:6) the compound appears to have a cage-like structure which is very similar to that which has been described in the literature for Cd–phytochelatin systems. However, at the lower mole ratios, the Cd–cys complexes show a tetrahedral geometry for the Cd:cys 1:4 complex. In addition, a tetrahedral geometry was also observed in the Cd:cys 1:2 complex, but the data suggests that there are two Cd ions sharing the S ligand of half of the cys. These Cd–cys compounds will provide valuable information on the binding mechanism of Cd in cys rich environments and the formation of phytochelatin/metallothionein complexes. Acknowledgements Portions of this research were carried out at the Stanford Synchrotron Radiation Laboratory, a national user facility operated by Stanford University on behalf of the U.S. Department of Energy, Office of Basic Energy Sciences. The SSRL Structural Molecular Biology Program is supported by the Department of Energy, Office of Biological and Environmental Research, and by the National Institutes of Health, National Center for Research Resources, Biomedical

Technology Program. This material is based upon work supported by the National Science Foundation and the Environmental Protection Agency under Cooperative Agreement Number EF 0830117. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation or the Environmental Protection Agency. This work has not been subjected to EPA review and no official endorsement should be inferred. J.L. Gardea-Torresdey also acknowledges the USDA grant # 2008-38422-19138, the LERR and STARs programs of the UT System and the Dudley family for the Endowed Research Professorship in Chemistry. J.G. Parsons would like to acknowledge NIH UTPA RISE program (Grant Number 1R25GM100866-01), NSF, URM program (grant number DBI 9034013), HHMI (grant 52007568). The Authors acknowledge financial support from the Welch Foundation for supporting the Department of Chemistry (Grant number GB-0017). References [1] I.J. Pickering, R.C. Prince, G.N. George, W.E. Rauser, W.A. Wickramasinghe, A.A. Watson, C.T. Damerson, I.G. Dance, D.P. Fairlie, D.E. Salt, Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1429 (1999) 351. [2] K. Shah, J.M. Nongkynrih, Biol. Plant. 51 (2007) 618. [3] A.I.G. Lima, S.I. Almeida Pereira, E.M. de Almeida Paula Figueira, G. Cardoso Nunes Caldeira, H.D. Quinteira de Matos Caldeira, Environ. Exp. Bot. 55 (2006) 149. [4] G.N. Babu, R. Ranjani, G. Fareeda, S.D.S. Murthy, J. Phytol. Res. 20 (2007) 1. [5] C.S. Cobbett, Plant Physiol. 123 (2000) 825. [6] M. Enescu, J.-P. Renault, S. Pommeret, J.-C. Mialocq, S. Pin, Phys. Chem. Chem. Phys. 5 (2003) 3762. [7] D.A. Fowle, M.J. Stillman, J. Biomol. Struct. Dyn. 14 (1997) 393. [8] J. Chan, M.E. Merrifield, A.V. Soldatov, M.J. Stillman, Inorg. Chem. 44 (2005) 4923. [9] P.J. Barrie, A. Gyani, M. Motevalli, P. O’Brien, Inorg. Chem. 32 (1993) 3862. [10] F. Jalilehvand, B.O. Leung, V. Mah, Inorg. Chem. 48 (2009) 5758. [11] F. Jalilehvand, V. Mah, B.O. Leung, J. Mink, G.M. Bernard, L. Hajba, Inorg. Chem. 48 (2009) 4219. [12] T. Ressler, J. Synchrotron Radiat. 5 (1998) 118. [13] J.G. Parsons, M.V. Aldrich, J.L. Gardea-Torresdey, Appl. Spectrosc. Rev. 37 (2002) 187. [14] A.L. Ankudinov, B.J. Ravel, J.J. Rehr, S.D. Conradson, Phys. Rev. B 58 (1998) 7565. [15] B.J. Ravel, J. Synchrotron Radiat. 8 (2001) 314. [16] A.W. Stevenson, M. Milanko, Z. Barnea, Acta Crystallogr., Sect. B 40 (1984) 521. [17] J. Laugier, B. Bochu, CHECKCELL: A Software Performing Automatic Cell/Space Group Determination. Collaborative Computational Project, Number 14 (CCP14), Laboratory of Materials and Physical Engineering, School of Physics, University of Grenoble, France. [18] K.M. Dokken, J.G. Parsons, J. McClure, J.L. Gardea-Torresdey, Inorg. Chim. Acta 362 (2008) 395. [19] S. Lacelle, W.C. Stevens, D.M. Kurtz Jr, J.W. Richardson Jr., R.A. Jacobson, Inorg. Chem. 23 (1984) 930. [20] T. Arai, T. Ikemoto, A. Hokura, Y. Terada, T. Kunito, S. Tanabe, I. Nakai, Environ. Sci. Technol. 38 (2004) 6468. [21] A.I. Frenkel, A. Vairavamurthy, M. Newville, J. Synchrotron Rad. 8 (2001) 669. [22] K.A. Kerr, J.P. Ashmore, Acta Crystallogr., Sect. B 29 (1973) 2124. [23] M.M. Harding, H.A. Long, Acta Crystallogr., Sect. B 24 (1968) 1096. [24] H.A. Castillo-Michel, N. Hernandez, A. Martinez-Martinez, J.G. Parsons, J.R. Peralta-Videa, J.L. Gardea-Torresdey, Plant Physiol. Biochem. 47 (2009) 608. [25] R.A. Santos, E.S. Gruff, S.A. Koch, G.S. Harbison, J. Am. Chem. Soc. 112 (1990) 9257. [26] S.J. Amberson, F.W.B. Einstein, P.C. Hayes, R. Kumar, D.G. Tuck, Inorg. Chem. 25 (1986) 4181. [27] P. De Meester, D.J. Hodgson, J. Chem. Soc., Dalton Trans. 7 (1976) 618. [28] N. Baidya, D. Ndreu, M.M. Olmstead, P.K. Mascharak, Inorg. Chem. 30 (1991) 2448.