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Ultrafast dynamics of heme distortion in the O₂-sensor of a thermophilic anaerobe bacterium

Petrova, Olga N. and Yoo, Byung-Kuk and Lamarre, Isabelle and Selles, Julien and Nioche, Pierre and Negrerie, Michel (2021) Ultrafast dynamics of heme distortion in the O₂-sensor of a thermophilic anaerobe bacterium. Communications Chemistry, 4 (1). Art. No. 31. ISSN 2399-3669. doi:10.1038/s42004-021-00471-9.

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Heme-Nitric oxide and Oxygen binding protein domains (H-NOX) are found in signaling pathways of both prokaryotes and eukaryotes and share sequence homology with soluble guanylate cyclase, the mammalian NO receptor. In bacteria, H-NOX is associated with kinase or methyl accepting chemotaxis domains. In the O₂-sensor of the strict anaerobe Caldanaerobacter tengcongensis (Ct H-NOX) the heme appears highly distorted after O₂ binding, but the role of heme distortion in allosteric transitions was not yet evidenced. Here, we measure the dynamics of the heme distortion triggered by the dissociation of diatomics from Ct H-NOX using transient electronic absorption spectroscopy in the picosecond to millisecond time range. We obtained a spectroscopic signature of the heme flattening upon O₂ dissociation. The heme distortion is immediately (<1 ps) released after O₂ dissociation to produce a relaxed state. This heme conformational change occurs with different proportions depending on diatomics as follows: CO < NO < O₂. Our time-resolved data demonstrate that the primary structural event of allostery is the heme distortion in the Ct H-NOX sensor, contrastingly with hemoglobin and the human NO receptor, in which the primary structural events are respectively the motion of the proximal histidine and the rupture of the iron-histidine bond.

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Yoo, Byung-Kuk0000-0002-2610-6685
Nioche, Pierre0000-0001-7981-9163
Alternate Title:Ultrafast dynamics of heme distortion in the O2-sensor of a thermophilic anaerobe bacterium
Additional Information:© The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit Received 25 September 2020; Accepted 05 February 2021; Published 05 March 2021. P.N. was supported by an Avenir starting grant, Region Ile-de-France under a CODDIM contract, an INSERM-Paris Descartes University Chaire mixte. O.N.P. was supported by an “Initiative Doctorale Interdisciplinaire” PhD fellowship from Université Paris-Saclay. Data availability: The authors declare that all data supporting the findings of this study are included in the main manuscript file or Supplementary Information or are available from the corresponding author upon request. Author Contributions: M.N. conceived and designed the research. P.N. produced and purified the protein. I.L. and O.N.P. performed biochemical analysis. O.N.P., B.-K.Y., and J.S. performed time-resolved measurements. M.N., O.N.P., and B.-K.Y. analyzed the data. M.N. and O.N.P. prepared the figures and wrote the manuscript. All authors approved the final version of the manuscript. The authors declare no competing interests.
Funding AgencyGrant Number
Région Île-de-FranceUNSPECIFIED
Institut national de la santé et de la recherche médicale (INSERM)UNSPECIFIED
Université Paris-SaclayUNSPECIFIED
Subject Keywords:Optical spectroscopy; Structural biology
Issue or Number:1
Record Number:CaltechAUTHORS:20210413-123137748
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Official Citation:Petrova, O.N., Yoo, BK., Lamarre, I. et al. Ultrafast dynamics of heme distortion in the O2-sensor of a thermophilic anaerobe bacterium. Commun Chem 4, 31 (2021).
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:108715
Deposited By: Tony Diaz
Deposited On:13 Apr 2021 22:18
Last Modified:13 Apr 2021 22:18

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