How Does Mg Interact with ATP? Biomolecular Structure through the Lens of Liquid-Jet Photoemission Spectroscopy.

Liquid-jet photoemission spectroscopy (LJ-PES) allows for a direct probing of electronic structure in aqueous solutions. We show the applicability of the approach to biomolecules in a complex environment, exploring site-specific information on the interaction of adenosine triphosphate in the aqueous phase (ATP) with magnesium (Mg), highlighting the synergy brought about by the simultaneous analysis of different regions in the photoelectron spectrum. In particular, we demonstrate intermolecular Coulombic decay (ICD) spectroscopy as a new and powerful addition to the arsenal of techniques for biomolecular structure investigation. We apply LJ-PES assisted by electronic-structure calculations to study ATP solutions with and without dissolved Mg. Valence photoelectron data reveal spectral changes in the phosphate and adenine features of ATP due to interactions with the divalent cation. Chemical shifts in Mg 2p, Mg 2s, P 2p, and P 2s core-level spectra as a function of the Mg/ATP concentration ratio are correlated to the formation of [Mg(ATP) ], [MgATP], and [MgATP] complexes, demonstrating the element sensitivity of the technique to Mg-phosphate interactions. The most direct probe of the intermolecular interactions between ATP and Mg is delivered by the emerging ICD electrons following ionization of Mg 1s electrons. ICD spectra are shown to sensitively probe ligand exchange in the Mg-ATP coordination environment. In addition, we report and compare P 2s data from ATP and adenosine mono- and diphosphate (AMP and ADP, respectively) solutions, probing the electronic structure of the phosphate chain and the local environment of individual phosphate units in ATP. Our results provide a comprehensive view of the electronic structure of ATP and Mg-ATP complexes relevant to phosphorylation and dephosphorylation reactions that are central to bioenergetics in living organisms.