Unraveling the Mechanisms of Nonradiative Deactivation in Model Peptides Following Photoexcitation of a Phenylalanine Residue

Abstract

The mechanisms of nonradiative deactivation of a phenylalanine residue after near-UV photoexcitation have been investigated in an isolated peptide chain model (N-acetylphenylalaninylamide, NAPA) both experimentally and theoretically. Lifetime measurements at the origin of the first ππ* state of jet-cooled NAPA molecules have shown that (i) among the three most stable conformers of the molecule, the folded conformer NAPA B is ∼50-times shorter lived than the extended major conformer NAPA A and (ii) this lifetime is virtually insensitive to deuteration at the NH(2) and NH sites. Concurrent time-dependent density functional theory (TDDFT) based nonadiabatic dynamics simulations in the full dimensionality, carried out for the NAPA B conformer, provided direct insights on novel classes of ultrafast deactivation mechanisms, proceeding through several conical intersections and leading in fine to the ground state. These mechanisms are found to be triggered either (i) by a stretch of the N(Phe)H bond, which leads to an H-transfer to the ring, or (ii) by specific backbone amide distortions. The potential energy surfaces of the NAPA conformers along these critical pathways have been characterized more accurately using the coupled cluster doubles (CC2) method and shown to exhibit barriers that can be overcome with moderate excess energies. These results analyzed in the light of the experimental findings enabled us to assign the short lifetime of NAPA B conformer to a number of easily accessible exit channels from the initial ππ* surface, most importantly the one involving a transfer of electronic excitation to an nπ* surface, induced by distortions of the backbone peptide bond.

Isolated Neutral Peptides

“…Only a few experimental studies suggest that the excited-state lifetime could be much shorter than the radiative lifetime. Thus conformer-dependent lifetimes in the 1-80 ns range have been reported at the origin of the first ππ* transition of isolated natural Phe [75,91] as well as of a more biologically relevant capped amino-acid [110,115,200], for which quantum chemical calculations have shown that peptide bond nπ* states are responsible for the lifetime shortening observed. Still shorter (sub-nanosecond) lifetimes are out of reach of the techniques employed, but are suspected to occur in the hydrates of capped Phe [200], suggesting that detection by ns-UV excitation might become a concern.…”

“…Such a situation has not yet been revealed on peptides, only lifetimes strongly varying with conformation in the nanosecond regime having been encountered. These measurements are scarce and are limited to Phe-based peptides [75,91,110,115] and Tyr [56]. In a few peptiderelated compounds, presenting a phenyl chromophore and an amide group, short monomer lifetimes are suspected [18].…”

Tyrosine-glycine revisited: Resolving the discrepancy between theory and experiment

“…Highly efficient non-radiative relaxation pathways for excited states of hydrogen-bonded peptide conformers were recently proposed by Mališ et al [23] A folded conformer of N-acetylphenylalaninylamide (NAPA), containing two intramolecular H-bonds (one of the NH•••O type, the other an NH-π bond between the N Phe H bond and the phenyl ring), was revealed by R2PI experiments to have a short excited-state lifetime (~1.5 ns). This explained its absence from earlier laser-induced fluorescence studies.…”

UV–UV hole burning and IR dip spectroscopy of homophenylalanine by laser desorption supersonic jet technique

“…In the former report, [22] excited state dynamics of each conformer of Phe were experimentally investigated and it was demonstrated that S 1 state lifetimes differ among conformers. Furthermore, for the peptides, it has been reported that the excited state dynamics are strongly affected by the conformations [38,39]. Thus it will be interesting to compare the photophysical properties such as lifetime between similar conformers of HPhe and Phe.…”