Femtosecond X-ray emission study of the spin cross-over dynamics in haem proteins
Dominik Kinschel, Camila Bacellar, Oliviero Cannelli, Boris Sorokin, Tetsuo Katayama, Giulia F. Mancini, Jérémy R. Rouxel, Yuki Obara, Junichi Nishitani, Hironori Ito, Terumasa Ito, Naoya Kurahashi, Chika Higashimura, Shotaro Kudo, Theo Keane, Frederico A. Lima, Wojciech Gawelda, Peter Zalden, Sebastian Schulz, James M. Budarz, Dmitry Khakhulin, Andreas Galler, Christian Bressler, Christopher J. Milne, Thomas Penfold, Makina Yabashi, Toshinori Suzuki, Kazuhiko Misawa, Majed Chergui
Abstract
Abstract In haemoglobin the change from the low-spin (LS) hexacoordinated haem to the high spin (HS, S = 2) pentacoordinated domed deoxy-myoglobin (deoxyMb) form upon ligand detachment from the haem and the reverse process upon ligand binding are what ultimately drives the respiratory function. Here we probe them in the case of Myoglobin-NO (MbNO) using element- and spin-sensitive femtosecond Fe K α and K β X-ray emission spectroscopy at an X-ray free-electron laser (FEL). We find that the change from the LS (S = 1/2) MbNO to the HS haem occurs in ~800 fs, and that it proceeds via an intermediate (S = 1) spin state. We also show that upon NO recombination, the return to the planar MbNO ground state is an electronic relaxation from HS to LS taking place in ~30 ps. Thus, the entire ligand dissociation-recombination cycle in MbNO is a spin cross-over followed by a reverse spin cross-over process.