Electronic landscape of the P-cluster of nitrogenase as revealed through many-electron quantum wavefunctions

TL;DR

This study uses advanced many-electron wavefunction simulations to reveal the complex electronic states and spin configurations of the nitrogenase P-cluster across different oxidation states, providing new insights into its role in nitrogen fixation.

Contribution

The paper introduces new theoretical methods enabling detailed characterization of the P-cluster's electronic structure, previously resistant to such analysis.

Findings

Dense spectrum of low-energy electronic states with overlapping orbital and spin excitations

Clusters exhibit superpositions of spin configurations with non-classical correlations

Oxidation increases the density of states, affecting electron transfer understanding

Abstract

The electronic structure of the nitrogenase metal cofactors is central to nitrogen fixation. However, the P-cluster and iron molybdenum cofactor, each containing eight irons, have resisted detailed characterization of their electronic properties. Through exhaustive many-electron wavefunction simulations enabled by new theoretical methods, we report on the low-energy electronic states of the P-cluster in three oxidation states. The energy scales of orbital and spin excitations overlap, yielding a dense spectrum with features we trace to the underlying atomic states and recouplings. The clusters exist in superpositions of spin configurations with non-classical spin correlations, complicating interpretation of magnetic spectroscopies, while the charges are mostly localized from reorganization of the cluster and its surroundings. Upon oxidation, the opening of the P-cluster significantly increases the density of states, which is intriguing given its proposed role in electron transfer. These results demonstrate that many-electron simulations stand to provide new insights into the electronic structure of the nitrogenase cofactors.