Direct Structural and Chemical Characterization of the Photolytic

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Spectroscopy and Photochemistry; General Theory

Direct Structural and Chemical Characterization of the Photolytic Intermediates of Methylcobalamin Using Time-Resolved X-ray Absorption Spectroscopy Ganesh Subramanian, Xiaoyi Zhang, Gerdenis Kodis, Qingyu Kong, Cunming Liu, Andrew V. G. Chizmeshya, Uwe Weierstall, and John C.H. Spence J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.8b00083 • Publication Date (Web): 06 Mar 2018 Downloaded from http://pubs.acs.org on March 9, 2018

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The Journal of Physical Chemistry Letters

Direct Structural and Chemical Characterization of the Photolytic Intermediates of Methylcobalamin Using Time-Resolved X-ray Absorption Spectroscopy Ganesh Subramanian,1 Xiaoyi Zhang,2 Gerdenis Kodis,3 Qingyu Kong,2 Cunming Liu, 2 Andrew Chizmeshya,3 Uwe Weierstall,1 and John Spence1, * 1

Department of Physics, Arizona State University, Tempe, Arizona 85287, USA

2

X-ray Sciences Division, Argonne National Laboratory, 9700 South Cass Avenue, Argonne,

Illinois 60439, USA 3

School of Molecular Sciences, Arizona State University, Tempe, Arizona 85287, USA

CORRESPONDING AUTHOR * John C. H. Spence. F.R.S. Richard Snell Professor of Physics. Director of Science, NSF BioXFEL STC. Department of Physics, Arizona State University. Tempe, AZ 85287-1504 USA. FAX: (480) 965-7954 Telephone: (480) 965-6486) [email protected] Dec 24, 2017.

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ABSTRACT: Cobalt-carbon bond cleavage is crucial to most natural and synthetic applications of the cobalamin class of compounds and here we present the first direct electronic and geometric structural characteristics of intermediates formed following photoexcitation of methylcobalamin (MeCbl) using time-resolved X-ray absorption spectroscopy (XAS). We catch transients corresponding to two intermediates, in the hundreds of picosecond (ps) and a few microsecond (µs) respectively. Highlights of the ps intermediate, which is reduced in comparison to the ground state, are elongation of the upper axial Co-C bond and relaxation of the corrin ring. This is not so with the recombining photocleaved products captured at a few µs, where the Co-C bond almost (yet not entirely) reverts to its ground state configuration and a substantially elongated lower axial Co-NIm bond is observed. The reduced cobalt site here confirms formation of methyl radical as the photoproduct.

TOC GRAPHIC

KEYWORDS: Co-C, photolysis, coordination, XANES, fine structure

Cleavage of the cobalt-carbon (Co-C) bond is central to the catalytic activity of cobalt corrinoids in the cobalamin (Vitamin B12) family.

1–3

There have been several efforts to


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investigate the reaction mechanism and pathway of this bond cleavage, mostly using optical transient absorption where the laser pump pulse initiates an electronic excited state and timedelayed probe pulses monitor the progress of the Co-C bond photolysis.

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Methylcobalamin

(MeCbl) is the cofactor (form of cobalamin) that participates in the methyl-transfer cycle within the human body.

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Photolysis of MeCbl is expected to proceed via different mechanisms

depending on the excitation wavelength (energy) of the laser pump pulse. 6 Sension et al 7 have proposed that with 400 nm incident wavelength, the MeCbl molecules split into two fractions with a ¼ chance of undergoing prompt homolysis and ¾ chance of a heterolytic intermediate. Using the transient optical absorption signature of a blue-shifted gamma band at 340 nm (suggesting either a weakly bound or completely detached 5-coordinate Co(III) cation and a carbanion) and a red-shifted alpha/beta band at 550 nm (matching closely with position of the alpha band in CNCbl), the heterolytic species is characterized as a charge-separated CoIII intermediate. This intermediate largely recombines to the ground state with a small fraction evolving to form cob(II)alamin and methyl radical similar to (and adding to) the prompt homolysis as photoproducts. The latter largely recombine to the ground state on a µs time scale or form irreversible photoproducts that accumulate in time (refer fig. S1 in SI for reaction schematic). Theoretical studies in past decades have used density functional theory (DFT) and timedependent DFT (TD-DFT) as tools to simulate for the energy surfaces of the ground state and photo-excited intermediates to map out a possible reaction mechanism for the photolysis of MeCbl.

8–10

Kozlowski et al

8

have performed systematic TD-DFT analyses on the cobalamin

family and report that for the base-on form of MeCbl, 400 nm excitation populates the S7-S9 electronic excited states. In relaxing from the electronic excited state, the system’s first structural


3


response

is

the

elongation

of

its

lower

axial

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cobalt-nitrogen

(bound

to

the

dimethylbenzimidazole, Co-NDBI) bond followed by elongation of the upper axial Co-C bond leading to complete detachment of the upper axial bond (ref

9

fig. 5 Path B). The final

photoproduct is predicted to be a Co(II) radical with both its axial bonds detached. Other studies including EPR

11,12

and time-resolved IR

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broadly support these findings.

Nevertheless, there is a critical need for complementary experiments capable of directly probing both structural and chemical changes of the intermediates during the photochemical reaction, in order to fully elucidate and confirm these findings. High energy X-rays and electrons as probe offer the advantage of providing very high spatial resolution and/or element-specific chemical information. Time-resolved measurements using optical pump and X-ray probe absorption spectroscopy enable systematic characterization of the local coordination, relative oxidation change, ligation and bond strengths around the probe atom. More importantly, the latter approach furnishes valuable information about the electronic and geometric structure of both steady-states and transient intermediates.

14,15

Recently, time-

resolved XAS study at ultrafast timescales on cyanocobalamin (CNCbl) was performed using a free-electron X-ray laser

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that highlights the structure and nature of charge transfer of excited

states formed a few hundreds of femtoseconds (fs) to several ps after optical excitation. In this work, we adopt a similar approach to study the intermediates formed during the photolysis of MeCbl. Since there are no prior time-resolved X-ray measurements on MeCbl beyond the millisecond regime,

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our study characterizes the photoinduced intermediates in the

hundreds of ps and slower timescales, now accessible using third generation synchrotrons. Optical laser pulses centered at 400 nm were used to photoexcite MeCbl molecules dissolved in


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water at pH7 and 1mM concentration. These molecules were probed by hard X-rays at the cobalt K-edge to obtain the X-ray absorption spectra before and after excitation. In corroboration, molecular structures obtained from DFT calculations were used to obtain the simulated X-ray absorption spectra for further analysis. (Refer to SI for details on methods)

Figure 1: (a) Pre-laser exposure (solid black) and post-laser exposure (dotted black) steady-state XANES experimental spectrum of MeCbl. (b) Reference steady-state XANES experimental spectra of MeCbl (solid black) and OHCbl (dotted black). Labels for fine-structure features, (A) Pre-edge peak, (B) edge-kink, (C) rising absorption edge, (D) Shoulder peak, (E) Main absorption peak, (F) Multiple Scattering immediately post-edge and (G) Multiple Scattering farther post-edge.

Figure 1(a) shows the steady-state X-ray absorption near edge structure (XANES) spectra of the reactant (MeCbl) and post-laser excitation product. Since MeCbl is known to form a small fraction of irreversible products after photoexcitation (that would accumulate in time) we measured the absorption spectra of a few reference compounds. We notice a clear match of the


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OHCbl spectrum in Fig. 1(b) to that of the product in fig. 1(a). The near-edge fine structure of OHCbl is uniquely defined in comparison to other common cobalamins and hence we can unambiguously match the photoproduct and confirm the substitution of methyl- ligand. However, prior work suggests that OHCbl is a very basic form of the cobalamin and the pKa for conversion of AqCbl to OHCbl (acid-base) is about 7.8

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which means at pH7 we characterize

the product to majorly contain an aqua-ligated (AqCbl) cobalamin. In the XANES portion of the spectrum, seven features have been identified as finestructure, labeled A through G. Qualitative assessment immediately highlights a few features of the product spectra (Fig. 1a) in comparison to the reactant – (i) the intensity of the pre-edge feature (A) of the product is substantially reduced: The pre-edge feature is known to be an indicator of d-p mixing and also of the extent of centrosymmetry 19 about the core-excited atom. Reduced pre-edge intensity indicates the formation of a product species that is strongly centrosymmetric, maintaining the octahedral coordination. (ii) The edge onset (C) is blue-shifted (higher energies): the shift of the ionization edge reflects a relative change in the oxidation state 20

of the probed atom, and shift to higher energies indicates a cobalt atom that is more oxidized

in the product. So qualitative analysis identifies AqCbl to be a strongly symmetric octahedral molecule that is more oxidized than MeCbl.


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Figure 2: Optical pump – X-ray probe difference absorption spectra: 200 picoseconds time delay in GREEN and a few microseconds time delay in BLUE. BLACK: Steady-state MeCbl pH7 XANES spectrum for correlation. YELLOW BOX: Highlights the positive difference intensity at the absorption edge indicating reduced oxidation state of cobalt.

Following the steady-state measurements, we next measured intermediates of the photolysis reaction (refer to S6 in S1 for the optical transient measurements). Fig. 2 shows the transient spectra collected at 200 ps (green) and a few µs (blue) time-delays. These difference spectra show the changes in spectral features obtained by subtracting the XANES signal with laser OFF (ground state reactant) from that with laser ON (photoexcited state). Qualitative analysis of the transient spectra show: (i) Negative difference intensity at pre-edge (feature A): similar to steady-state product, the centrosymmetry is observed to increase. This could be interpreted as either a strongly symmetric octahedral or a square-planar symmetry. (ii) Rising edge (feature C) changes are strongly positive: positive changes in difference spectra here indicate that the ionization edge of the ‘laser ON’ spectrum is red-shifted. This suggests that the oxidation state of the cobalt center is reduced in comparison to the ground state. (iii) Edge kink (feature B) intensity increases: the small “kink” at the lower energy end of the rising edge in the ground state spectrum increases in intensity at the ps timescale and similarly in the µs timescale, with a much more pronounced change. This peak is generally attributed to 1s-4pz type transitions,

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which are more evident in a square-planar geometry since both the axial ligating

sites are vacant. In our transient spectra, this could indicate to the formation of a square planar intermediate or reiterate the elongated (weak) axial bonds of an octahedral molecule. The changes observed thus far (features A-C) are observed at the 200 ps timescale and extend well into the µs timescale. The following changes (features D-G), however, are non-trivial for direct interpretation and show varied behaviors at different timescales: (iv) Shoulder-peak (feature D)


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intensity change is positive and observed at ps times and absent in the µs timescale. (v) Main absorption peak (feature E) shows marginal reduction in intensity at ps and no significant change at µs (which could indicate relaxation towards reverting to the ground state conformation). (vi) Multiple scattering (MS) beyond the main peak (features F and G) show a change which is negative at ps and negligible at µs: Immediately past the ionization edge, the kinetic energy of the ejected photoelectron is small. This corresponds to scattering paths that could result from different combinations of trajectories of the emitted photoelectron and not just the first coordination shell. To gain a deeper understanding of the experimental XANES features, we performed DFT calculations using Gaussian09

21

to model the ground state reactant. Subsequently, we fed this

optimized structure to the ORCA program

22,23

(pre-edge) and the FEFF8.4 code

24

(edge and

post-edge) to simulate the XANES spectra. The truncated optimized structure from DFT and the corresponding coordinates for base on/off (pH7/pH2) MeCbl are presented in figures S2, S3 (SI) and Tables T1, T2 (SI) respectively. Figure S4 (SI) shows the comparison of the experimental (TOP) and the DFT+FEFF/ORCA-XAS simulated (BOTTOM) spectra of ground state MeCbl respectively. Using the arrow-heads as guidelines, it is evident that the changes noticed in the experimental spectra are reproduced in the simulations. To analyze the transient experimental spectra, we must identify the site/ligand specific origins of near edge fine-structure features of MeCbl. In this regard, distances of the two axial and in-plane bonds (all within the first coordination sphere) were varied systematically for the XANES simulation. A similar approach was used in understanding the XANES spectra of Myoglobin in the work by Lima et al. 25 Note that while one bond-length was modified, the rest


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of the structure was kept at the optimized ground state configuration (the molecule was not relaxed as a response to the altered bond-length).

Figure 3: Evolution of the simulated XANES fine-structure features of MeCbl for systematic increase in the bond-lengths of the first shell nearest neighbors to cobalt as (a) Co-Ncorrin bond with four cobalt to in-plane nitrogens (two each sharing one bond-distance) (b) upper axial Co-C bond and (c) lower axial Co-NIm bond. In each panel (i) inset in the top-left: corresponds to the ORCA simulated pre-edge spectrum (ii) inset in the bottom-right: in pink corresponds to the DFT optimized bond-length. For each iteration of modified bond-length, the rest of the structure was not re-optimized. Arrowheads guide the change of feature with increasing bond-distances.


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Figures. 3(a, b and c) represent the evolution of the XANES (shades of green from dark to light) of the ground state pH7 MeCbl molecule as a function of increasing bond-length of (a) the cobalt to in-plane corrin nitrogens (Co-Ncorrin) corresponding to the first coordination (b) upper axial Co-C bond and (c) lower axial Co-NIm bond. The simulated spectrum in pink (in each of the sub-panels of fig. 3 a, b and c) corresponds to the ground-state DFT optimized structure (refer T3 in SI). Tables T4 and T5 (SI) show the summary of simulated XANES changes (from figs. 3 a, b and c) tabulated to match experimental ps and µs difference spectra (fig. 2). A few unique relations stand out: (i) shoulder peak (D) intensity is strongly influenced by the upperaxial Co-C bond. (ii) MS immediately post edge at F seems to have a significant contribution only from the corrin nitrogens in plane. (iii) Shift of the main absorption peak E to different (lower) energies seems to be a unique contribution of the in-plane corrin nitrogens. Taking into account all of the above unique relations and others (see discussion of T4 and T5 in SI), we invoke the principle of Occam’s razor 26,27 to identify the structural composition of the intermediates in the ps and the µs timescales and a few related observations. (1) The ps intermediate represents a substantially elongated upper axial Co-C bond and a relaxed corrin ring around the cobalt atom with no significant change in the lower axial Co-NIm bond. This is consistent (and confirms) with prior experimental works 3,6,7 which characterize this intermediate as either a charge-separated ionic species or an upper axial detached 5-coordinate cobalt complex. Reduced pre-edge intensity (fig. 2 and fig. 3b inset) in the transient spectrum, however, indicates that upper axial Co-C bond elongation (and the relaxed corrin) actually improves the centrosymmetry about the cobalt atom forming a more symmetric octahedron as an intermediate. Note that the ps spectrum is a convolution of spectra from two intermediate species (as from fig. S6 and following text in SI). However, the spectral features are dominated by the major fraction


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corresponding to the charge-transfer intermediate (refer to fig. S7 in the SI for a detailed discussion regarding this assumption). (2) The µs intermediate shows clear signature of photoproducts on recombination pathway to form the reactant. The upper axial Co-C bond is marginally elongated, and all of the corrin in-plane nitrogens are back to their original configurations. Co-NIm is the only bond still sufficiently elongated from its steady state configuration. In the µs transient spectrum (fig. 2 blue), the intermediate is in a reduced oxidation state compared to the ground state. This is only possible if photocleavage creates •CH3 (a methyl radical and not a carbanion CH3¯) that could abstract more electron density from cobalt during recombination thereby oxidizing the cobalt atom. Our measurements thus not only confirm formation of the methyl radical as photoproduct but also confirm the need for two parallel pathways at the ps timescales (post excitation) considering one of them moves through a charge-transfer intermediate involving the carbanion formation (as proposed by Walker et al

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and as in fig. S1 in SI). In such a case, the second pathway (prompt homolysis) would primarily contribute to formation of the photocleaved radicals (refer to discussion around fig. S5 in SI). In summary, we utilize the technique of time-resolved optical-pump X-ray-probe absorption spectroscopy to obtain the first direct electronic and geometric structures of intermediates formed in the photolysis of methylcobalamin. We are able to capture two transient spectra at 200 ps and a few µs respectively. The ps intermediate displays a strong elongation of the upper axial Co-C bond, which is very poorly (but definitely) bound, accompanied by a marginal relaxation of the in-plane corrin ring. The lower axial Co-NIm remains relatively unchanged. In comparison to the reactant, this intermediate has reduced oxidation and stronger octahedral centrosymmetry. Once the photoproducts are generated, they either recombine to the ground state or form irreversible products. At the few µs timescale, we capture signatures of a


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molecule that has structurally almost reverted back to its ground state configuration with the exception of the axial ligands. The intermediate is still reduced in comparison to ground state suggesting that the recombining (hence photocleaved) component must be a methyl radical confirming prior assessments. In this case, the lower axial Co-NIm bond is substantially elongated while the upper axial Co-C bond is almost at its ground state configuration, although not entirely. The reaction product is confirmed as an aqua-substituted cobalamin. ASSOCIATED CONTENT Supporting Information. Details about the sample (procurement and preparation), experimental techniques (set-up and corresponding data analysis) and simulations (DFT and XAS) are presented as Supporting Information (SI). Transient optical studies and additional analysis of Xray data are also presented in the SI. AUTHOR INFORMATION Corresponding Author •

John Spence, E-mail: [email protected]

Notes The authors declare no competing financial interest.

ACKNOWLEDGEMENTS We acknowledge the NSF STC award 1231306 that supported the research. We would like to also thank Dr. Su Lin and the CLAS Ultrafast Laser Facility for access to the transient optical absorption set-up. We thank the High Performance Computing facility at ASU for all the computing hours utilized for the DFT calculations. This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for


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the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC0206CH11357.

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Direct Structural and Chemical Characterization of the Photolytic

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