Atomic and Electronic Structure of Pilus from Geobacter sulfurreducens through QM/MM Calculations: Evidence for Hole Transfer in Aromatic Residues

Abstract

Long-range electron transport has been widely and experimentally reported in Geobacter sulfurreducens pilus protein. However, a better understanding of the still undefined molecular arrangement can bring to light the role of key residues in this phenomenon. We propose a theoretical investigation of the electronic structure of aromatic residue groups in the protein through a classical molecular dynamics (MD) simulation, followed by a quantum mechanics/molecular mechanics (QM/MM) electronic study of different frames sampled from MD trajectories, an electrostatic potential and electron density analysis, an analysis of the density of states, and an investigation of hole formation through Dyson orbital calculations. We observe a highest occupied molecular orbital-lowest unoccupied molecular orbital (HOMO–LUMO) energy gap in the ranges of 1.4–2.3 eV and 2.9–3.3 eV and a less intense dipole moment along the aromatic residues in the presence of water in comparison to the system in vacuum. HOMO and LUMO electron densities highlight the occupation of one tyrosine residue in every representation for HOMO and a delocalization along two to three rings for LUMO. The results show how the electronic structure of the aromatic residues is sensitive to the ring arrangement and the surrounding environment. In our study, we observe that slight rearrangements in the fiber geometry can create temporary conditions for hole transfer.

Electronic Structure of de Novo Peptide ACC-Hex from First Principles

“…We speculate that temperature and disorder will be important for carrier transport. This is consistent with a flickering resonance electron transport as suggested Beratan and co-workers, , superexchange as suggested by Renaud and co-workers, , or both.…”

“…Notably, for MtrF (a protein complex with a chain of heme groups), thermally averaging the structure resulted in an increased electronic coupling by a factor 3 when compared to the T = 0 K structure . Additionally, studies of studies of hypothetical G. sulfurreducens pilin protein structures, considering three aromatic rings explicitly with quantum mechanics, showed that atomic vibrations via molecular mechanics result in a time-dependent change to the energy and ordering of molecular orbitals, with the hole diffusivity dependence on dephasing being strongly dependent on geometry . Here, we investigate the role of atomic vibrations on the energy and nature of near-gap states in ACC-Hex.…”

“…The conductivity regime is determined by the electronic and physical structure of the assembly. , The bandgap (energy difference between the highest occupied molecular orbital (HOMO) and lowest unoccupied molecular orbital (LUMO)), the bandwidth (or energy level spacing), and the localization of orbitals will significantly impact the conductivity regime and efficiency of long-range electron transport. The energetics and coherence of electronic states are in turn dependent on the physical structure of the system; for example, the distance and orientation between amino acids, and the presence and pH of the solution − can modify electronic coupling and the bandgap. Thus, it is necessary to understand the relationship between atomic structure, electronic structure, and conductivity.…”

“…Density functional theory (DFT) calculations have been successfully utilized to understand the electronic structure of bioelectronic materials. Often, these studies make an assumption that the electronic structure of a subsystem, comprising of atoms forming anticipated charge carrier sites, can be partitioned and treated at the DFT level, while the electronic effects of the surrounding medium are described with a less computationally demanding model, e.g., by force fields ,,, or homology. , Additionally, atomic vibrations associated with the subsystem and surrounding medium or bath can be incorporated in the theory to understand their role in reorganization energies, , structural properties, or coupling of subsystem to the phonon bath associated with the environment. , However, the majority of studies neglect orbital delocalization outside of the subsystem partition, which can be important for coherent transport (through-bond tunneling), , and the impacts of the environment (screening, electronic delocalization on side chains), which can impact electronic coupling. ,, …”

Heme Hopping Falls Short: What Explains Anti-Arrhenius Conductivity in a Multi-heme Cytochrome Nanowire?

“…In the absence of atomic-scale structural data until very recently (Figure 1, top middle ), 50 this suggestion spurred the creation of model systems 59–69 and theoretical studies based on homology modeling, docking, and molecular dynamics. 70–80 Computed conductivities for the hypothetical pilus have ranged from orders of magnitude too small 73 to quantitatively accurate 77 relative to experimental measurements attributed to the pilus. Proposed mechanisms include multistep hopping between aromatic sidechains, 72 transport through aromatic clusters with delocalized states, 76 or aromatic sidechains and cytochromes thought to decorate the pili, 71 or band-like conductivity through π-π stacked aromatic residues.…”