Low-energy spectrum of iron-sulfur clusters directly from many-particle quantum mechanics

TL;DR

This paper presents the first direct quantum mechanical calculations of the electronic energy levels of iron-sulfur clusters, revealing limitations of traditional models and explaining their biological ubiquity.

Contribution

It provides novel, model-free quantum calculations of FeS clusters' electronic states, challenging existing models and explaining their biological prevalence.

Findings

Heisenberg-Double-Exchange model underestimates states by 1-2 orders of magnitude.

Electronic energy levels are dense, facilitating catalytic reactivity.

Traditional models omit Fe d→d excitations, affecting accuracy.

Abstract

FeS clusters are a universal biological motif. They carry out electron transfer, redox chemistry, and even oxygen sensing, in diverse processes including nitrogen fixation, respiration, and photosynthesis. The low-lying electronic states are key to their remarkable reactivity, but cannot be directly observed. Here we present the first ever quantum calculation of the electronic levels of [2Fe-2S] and [4Fe-4S] clusters free from any model assumptions. Our results highlight limitations of long-standing models of their electronic structure. In particular, we demonstrate that the widely used Heisenberg-Double-Exchange model underestimates the number of states by 1-2 orders of magnitude, which can conclusively be traced to the absence of Fe d$\rightarrow$d excitations, thought to be important in these clusters. Further, the electronic energy levels of even the same spin are dense on the scale of vibrational fluctuations, and this provides a natural explanation for the ubiquity of these clusters in nature for catalyzing reactions.