The carbonyl-lock mechanism underlying non-aromatic fluorescence in biological matter

Abstract

Challenging the basis of our chemical intuition, recent experimental evidencereveals the presence of a new type of intrinsic fluorescence in biomoleculesthat exists even in the absence of aromatic or electronically conjugated che-mical compounds. The origin of this phenomenon has remained elusive so far.In the present study, we identify a mechanism underlying this new type offluorescence in different biological aggregates. By employing non-adiabatic abinitio molecular dynamics simulations combined with a data-driven approach,we characterize the typical ultrafast non-radiative relaxation pathways activein non-fluorescent peptides. We show that the key vibrational mode for thenon-radiative decay towards the ground state is the carbonyl elongation. Non-aromatic fluorescence appears to emerge from blocking this mode with stronglocal interactions such as hydrogen bonds. While we cannot rule out theexistence of alternative non-aromatic fluorescence mechanisms in other sys-tems, we demonstrate that this carbonyl-lock mechanism for trapping theexcited state leads to the fluorescence yield increase observed experimentally,and set the stage for design principles to realize novel non-invasive bio-compatible probes with applications in bioimaging, sensing, andbiophotonics.