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Ultrafast photoreduction dynamics of a new class of CPD photolyases

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Abstract

NewPHL is a recently discovered subgroup of ancestral DNA photolyases. Its domain architecture displays pronounced differences from that of canonical photolyases, in particular at the level of the characteristic electron transfer chain, which is limited to merely two tryptophans, instead of the "classical" three or four. Using transient absorption spectroscopy, we show that the dynamics of photoreduction of the oxidized FAD cofactor in the NewPHL begins similarly as that in canonical photolyases, i.e., with a sub-ps primary reduction of the excited FAD cofactor by an adjacent tryptophan, followed by migration of the electron hole towards the second tryptophan in the tens of ps regime. However, the resulting tryptophanyl radical then undergoes an unprecedentedly fast deprotonation in less than 100 ps in the NewPHL. In spite of the stabilization effect of this deprotonation, almost complete charge recombination follows in two phases of ~ 950 ps and ~ 50 ns. Such a rapid recombination of the radical pair implies that the first FAD photoreduction step, i.e., conversion of the fully oxidized to the semi-quinone state, should be rather difficult in vivo. We hence suggest that the flavin chromophore likely switches only between its semi-reduced and fully reduced form in NewPHL under physiological conditions.

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Acknowledgements

The present work has benefited from the platform of Biophysics of I2BC supported by French Infrastructure for Integrated Structural Biology (FRISBI) ANR-10-INBS-05.

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Authors and Affiliations

  1. PASTEUR, Département de Chimie, École Normale Supérieure, PSL University, CNRS, Sorbonne Université, 75005, Paris, France

    Fabien Lacombat, Agathe Espagne, Nadia Dozova & Pascal Plaza

  2. Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, CEA, CNRS, 91198, Gif-sur-Yvette, France

    Pavel Müller

  3. Department of Chemistry, Center for Synthetic Microbiology, Philipps University, 35032, Marburg, Germany

    Hans-Joachim Emmerich, Martin Saft & Lars-Oliver Essen

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  1. Fabien Lacombat
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  8. Lars-Oliver Essen
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Correspondence to Pascal Plaza, Pavel Müller or Lars-Oliver Essen.

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FOREWORD: This article is dedicated to Klaus Brettel on the occasion of his retirement. Klaus has played a major role in the careers of several authors of the present article. Mentor and dear friend for some of us, close collaborator for others, he has guided us and provided us with the example of research of the highest scientific level, conducted with unfailing rigor, most discerning standards and absolute honesty.

Pushing the limits of flash photolysis to unravel the secrets of biological electron and proton transfer - a topical issue in honour of Klaus Brettel.

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Lacombat, F., Espagne, A., Dozova, N. et al. Ultrafast photoreduction dynamics of a new class of CPD photolyases. Photochem Photobiol Sci 20, 733–746 (2021). https://doi.org/10.1007/s43630-021-00048-4

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  • DOI: https://doi.org/10.1007/s43630-021-00048-4

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