Specific versus Nonspecific Solvent Interactions of a Biomolecule in Water

TL;DR

This study combines experimental and theoretical methods to reveal a specific hydrogen-bonding motif of indole in water, showing detailed solvent interactions crucial for understanding biomolecular hydration.

Contribution

It uncovers a specific N-H...OH2 hydrogen bond motif in indole-water interactions using combined spectroscopic and ab initio modeling techniques.

Findings

Identified a strong localized N-H...OH2 hydrogen bond in indole-water systems.

Quantitatively explained X-ray photoemission and Auger spectra of aqueous indole.

Highlighted the role of specific hydrogen bonds in biomolecular hydration.

Abstract

Solvent interactions, particularly hydration, are vital in chemical and biochemical systems. Model systems unveil microscopic details of such interactions. We uncover a specific hydrogen-bonding motif of the biomolecular building block indole (C$_8$H$_7$N), tryptophan's chromophore, in water: a strong localized $\text{N-H}\cdots\text{OH}_2$ hydrogen bond, alongside unstructured solvent interactions. This insight is revealed from a combined experimental and theoretical analysis of indole's electronic structure in aqueous solution. We have recorded the complete X-ray photoemission and Auger spectrum of aqueous-phase indole, quantitatively explaining all peaks through \emph{ab initio} modeling. The efficient and accurate technique for modeling valence and core photoemission spectra involves the maximum-overlap method and the non-equilibrium polarizable-continuum model. A two-hole electron-population analysis quantitatively describes the Auger spectra. Core-electron binding energies for nitrogen and carbon highlight the specific interaction with a hydrogen-bonded water molecule at the N-H group and otherwise nonspecific solvent interactions.