Hydrogen Bonds Regulate Paramagnetic Spin Delocalization in Ferric Hemes

Hydrogen bonds in metalloprotein active sites regulate reactivity and facilitate electronic communication between metal centers and their surrounding environment. However, systematic control over hydrogen-bond-mediated spin delocalization has not been achieved in a synthetic system. Here, we combine experiment and theory to demonstrate that hydrogen bonds provide a tunable pathway for spin delocalization from a paramagnetic iron center into the distal secondary coordination sphere. Using a series of five-coordinate biphenolato Fe(III) porphyrin complexes with systematically varied hydrogen-bond strengths, we establish a well-defined noncovalent framework for controlling spin propagation. Paramagnetic 1H and 19F NMR spectroscopy reveals pronounced hyperfine shifts within the hydrogen-bonded distal environment, whereas no measurable spin delocalization is detected in analogous complexes lacking hydrogen bonds. Complementary DFT calculations reproduce the experimental spin-density distributions and show that hydrogen bonding functions as an effective ON/OFF switch for spin communication across a noncovalent interface. The strong correlation between hydrogen-bond strength, experimentally observed hyperfine shifts, and calculated spin densities establishes hydrogen bonding as a reversible and tunable conduit for spin communication beyond the primary coordination sphere. These findings provide direct insight into how subtle secondary-sphere interactions govern magnetic communication in paramagnetic systems and may operate as environment-responsive spin relays in biological redox centers.