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Femtosecond X-ray emission study of the spin cross-over dynamics in haem proteins

August 18, 2020

Physicists from Switzerland, Japan and Germany have unveiled the mechanism by which the first event of respiration takes place in heme proteins.

Respiration is a fundamental process of all living things, allowing them to produce energy, stay healthy, and survive. In cells, respiration involves what are known as “respiratory proteins”, e.g. hemoglobin in the blood and myoglobin in muscles. Respiratory proteins work by binding and releasing small molecules like oxygen, carbon monoxide etc., called ligands. They do this through their “active center”, which in many respiratory proteins is a chemical structure called heme porphyrin.

Binding and releasing small molecules causes changes in the heme’s molecular and electronic structure. Such a change is the transition from a planar low spin ligated porphyrin form to a domed high spin un-ligated form and vice-versa. This shift is a key step for respiration, ultimately switching hemoglobin between a “relaxed” and “tense” conformation.

Electrons spin around atoms, but also spin around themselves, and can cross over from one spin state to another. The debate about the transition from low-spin planar to a high-spin domed heme has been dominated by two schools of thought: the process is either by thermal relaxation or by a cascade among electron spin states.

Now, a team of scientists led by Majed Chergui at EPFL’s School of Basic Sciences have solved the debate. The researchers detached the small molecule from the heme using short, energizing laser pulses. They then used another short, hard X-ray pulse from an X-ray free-electron laser to induce X-ray emission (XES), a very sensitive fingerprint of the spin state of molecules, which monitored the heme’s changes as a function of time. They could thus determine that the passage from planar to domed and back is caused by a cascade among spin states.

Figure Experimental Scheme: a Energy level diagram showing the origin of the Kα and Kβ fluorescence after creation of a hole in the 1s (K) shell. The Kα1 and Kα2 lines originate from the splitting of the 2p orbital (2p1/2 and 2p3/2), whereas for Kβ these lines are degenerate, resulting in the line labelled Kβ1,3. b Experimental setup for the time-resolved X-ray emission spectroscopy measurements at the XFEL. The green line represents the optical (533 nm) pump pulse used to excite the sample and the red line represents the X-ray (centred at 8.168 keV) probe pulse at varying time delays (black arrow). The pulses are overlapped and intercept the sample at the green interaction region. A von Hamos geometry was used for these measurements.

See also: EurekAlert, Mirage News,
 
Reference: Kinschel, D., Bacellar, C., Cannelli, O., Sorokin, B., Katayama, T., Mancini, G.F., Rouxel, J.R., Obara, Y., Nishitani, J., Ito, H., Ito, T., Kurahashi, N., Higashimura, C., Kudo, S., Keane, T., Lima, F.A., Gawelda, W., Zalden, P., Schulz, S., Budarz, J.M., Khakhulin, D., Galler, A., Bressler, C., Milne, C.J., Penfold, T., Yabashi, M., Suzuki, T., Misawa, K., and Chergui, M. (2020). Femtosecond X-ray emission study of the spin cross-over dynamics in haem proteins. Nature Commun 11, 4145. (10.1038/s41467-020-17923-w)

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