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

Iron–sulfur 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. Their low-lying electronic states are key to their remarkable reactivity, but they 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 the 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 one to two orders of magnitude, which can conclusively be traced to the absence of Fe d d excitations, thought to be important in these clusters. Furthermore, 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 catalysis in nature. FeS clusters are a universal motif in organisms and are central to many processes, including nitrogen fixation and respiration. By carrying out the first many-electron calculation of the [2Fe-2S] and [4Fe-4S] clusters, they are shown to have an unusual set of closely packed energy levels, which are key to understanding their reactivity.