Probing the Excited State of Methylcobalamin Using Polarized Time-Resolved X-ray Absorption Spectroscopy

Michocki, Lindsay B.; Miller, Nicholas A.; Alonso-Mori, Roberto; Britz, Alexander; Deb, Aniruddha; Glownia, James M.; Kaneshiro, April K.; Konar, Arkaprabha; Koralek, Jake; Meadows, Joseph H.; Sofferman, Danielle L.; Song, Sanghoon; Toda, Megan J.; van Driel, Tim B.; Kozlowski, Pawel M.; Kubarych, Kevin J.; Penner-Hahn, James E.; Sension, Roseanne J.

doi:10.1021/acs.jpcb.9b05854

Title: Probing the Excited State of Methylcobalamin Using Polarized Time-Resolved X-ray Absorption Spectroscopy

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Abstract

We use picosecond time-resolved polarized X-ray absorption near-edge structure (XANES) measurements to probe the structure of the long-lived photoexcited state of methylcobalamin (MeCbl) and the cob(II)alamin photoproduct formed following photoexcitation of adenosylcobalamin (AdoCbl, coenzyme B12). For MeCbl, we used 520 nm excitation and a time delay of 100 ps to avoid the formation of cob(II)alamin. We find only small spectral changes in the equatorial and axial directions, which we interpret as arising from small (<~0.05 Å) changes in both the equatorial and axial distances. This confirms expectations based on prior UV–visible transient absorption measurements and theoretical simulations. We do not find evidence for the significant elongation of the Co–C bond reported by Subramanian [ J. Phys. Chem. Lett. 2018, 9, 1542–1546] following 400 nm excitation. For AdoCbl, we resolve the difference XANES contributions along three unique molecular axes by exciting with both 540 and 365 nm light, demonstrating that the spectral changes are predominantly polarized along the axial direction, consistent with the loss of axial ligation. These data suggest that the microsecond “recombination product” identified by Subramanian et al. is actually the cob(II)alamin photoproduct that is produced following bond homolysis of MeCbl with 400 nm excitation. Our results highlight themore »« less

Authors:

Michocki, Lindsay B. ^[1]; Miller, Nicholas A. ^[1]; Alonso-Mori, Roberto ^[2];

^[2];

^[3]; Glownia, James M. ^[2]; Kaneshiro, April K. ^[4];

^[5]; Koralek, Jake ^[2]; Meadows, Joseph H. ^[1]; Sofferman, Danielle L. ^[5]; Song, Sanghoon ^[2]; Toda, Megan J. ^[6]; van Driel, Tim B. ^[2];

^[6];

^[3];

^[3]

Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Chemistry and Biophysics
SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Chemistry and Biophysics, and Physics
Department of Biological Chemistry, University of Michigan, 1150 W. Medical Center Dr., Ann Arbor, Michigan 48109-0600, United States
Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Physics
Univ. of Kentucky, Lexington, KY (United States). Dept. of Chemistry

Publication Date:: Fri Jun 14 00:00:00 EDT 2019

Research Org.:: SLAC National Accelerator Lab., Menlo Park, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1560643

Grant/Contract Number:: 1428479; 1464584; 1608553; 1836435; 1565795; AC02-76SF00515

Resource Type:: Accepted Manuscript

Journal Name:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

Additional Journal Information:: Journal Volume: 123; Journal Issue: 28; Journal ID: ISSN 1520-6106

Publisher:: American Chemical Society

Country of Publication:: United States

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats


                    Michocki, Lindsay B., Miller, Nicholas A., Alonso-Mori, Roberto, Britz, Alexander, Deb, Aniruddha, Glownia, James M., Kaneshiro, April K., Konar, Arkaprabha, Koralek, Jake, Meadows, Joseph H., Sofferman, Danielle L., Song, Sanghoon, Toda, Megan J., van Driel, Tim B., Kozlowski, Pawel M., Kubarych, Kevin J., Penner-Hahn, James E., and Sension, Roseanne J. Probing the Excited State of Methylcobalamin Using Polarized Time-Resolved X-ray Absorption Spectroscopy.  United States: N. p., 2019. 
Web.  doi:10.1021/acs.jpcb.9b05854.

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                    Michocki, Lindsay B., Miller, Nicholas A., Alonso-Mori, Roberto, Britz, Alexander, Deb, Aniruddha, Glownia, James M., Kaneshiro, April K., Konar, Arkaprabha, Koralek, Jake, Meadows, Joseph H., Sofferman, Danielle L., Song, Sanghoon, Toda, Megan J., van Driel, Tim B., Kozlowski, Pawel M., Kubarych, Kevin J., Penner-Hahn, James E., & Sension, Roseanne J. Probing the Excited State of Methylcobalamin Using Polarized Time-Resolved X-ray Absorption Spectroscopy.  United States.  https://doi.org/10.1021/acs.jpcb.9b05854

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                    Michocki, Lindsay B., Miller, Nicholas A., Alonso-Mori, Roberto, Britz, Alexander, Deb, Aniruddha, Glownia, James M., Kaneshiro, April K., Konar, Arkaprabha, Koralek, Jake, Meadows, Joseph H., Sofferman, Danielle L., Song, Sanghoon, Toda, Megan J., van Driel, Tim B., Kozlowski, Pawel M., Kubarych, Kevin J., Penner-Hahn, James E., and Sension, Roseanne J. Fri .  
"Probing the Excited State of Methylcobalamin Using Polarized Time-Resolved X-ray Absorption Spectroscopy".  United States.  https://doi.org/10.1021/acs.jpcb.9b05854.  https://www.osti.gov/servlets/purl/1560643.

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@article{osti_1560643,

  title        = {Probing the Excited State of Methylcobalamin Using Polarized Time-Resolved X-ray Absorption Spectroscopy},

  author       = {Michocki, Lindsay B. and Miller, Nicholas A. and Alonso-Mori, Roberto and Britz, Alexander and Deb, Aniruddha and Glownia, James M. and Kaneshiro, April K. and Konar, Arkaprabha and Koralek, Jake and Meadows, Joseph H. and Sofferman, Danielle L. and Song, Sanghoon and Toda, Megan J. and van Driel, Tim B. and Kozlowski, Pawel M. and Kubarych, Kevin J. and Penner-Hahn, James E. and Sension, Roseanne J.},

  abstractNote = {We use picosecond time-resolved polarized X-ray absorption near-edge structure (XANES) measurements to probe the structure of the long-lived photoexcited state of methylcobalamin (MeCbl) and the cob(II)alamin photoproduct formed following photoexcitation of adenosylcobalamin (AdoCbl, coenzyme B12). For MeCbl, we used 520 nm excitation and a time delay of 100 ps to avoid the formation of cob(II)alamin. We find only small spectral changes in the equatorial and axial directions, which we interpret as arising from small (<~0.05 Å) changes in both the equatorial and axial distances. This confirms expectations based on prior UV–visible transient absorption measurements and theoretical simulations. We do not find evidence for the significant elongation of the Co–C bond reported by Subramanian [ J. Phys. Chem. Lett. 2018, 9, 1542–1546] following 400 nm excitation. For AdoCbl, we resolve the difference XANES contributions along three unique molecular axes by exciting with both 540 and 365 nm light, demonstrating that the spectral changes are predominantly polarized along the axial direction, consistent with the loss of axial ligation. These data suggest that the microsecond “recombination product” identified by Subramanian et al. is actually the cob(II)alamin photoproduct that is produced following bond homolysis of MeCbl with 400 nm excitation. Our results highlight the pronounced advantage of using polarization-selective transient X-ray absorption for isolating structural dynamics in systems undergoing atomic displacements that are strongly correlated to the exciting optical polarization.},

  doi          = {10.1021/acs.jpcb.9b05854},

  journal      = {Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry},

  number       = 28,

  volume       = 123,

  place        = {United States},

  year         = {Fri Jun 14 00:00:00 EDT 2019},

  month        = {Fri Jun 14 00:00:00 EDT 2019}

}

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