Atomistic Modeling of Bio-Nano Hybrids: Interactions between Iron Oxide Nanoparticles and the Outer Membrane of <i>Shewanella</i>

Dissimilatory metal-reducing bacteria transfer electrons to the external surface of metal oxides during their anaerobic respiration. Combining these bacteria with iron oxide nanoparticles (NPs) supports continuous redox processes for bioremediation and bioenergy, yet their molecular interactions between iron oxide NPs and the extracellular membrane, which regulate extracellular electron transfer, remain unexplored. This work investigates the adsorption of an iron oxide (α-Fe₂O₃) NP with a 3.6 nm diameter onto the outer membrane (OM) of <i>Shewanella</i> in the absence of lipopolysaccharide (LPS) and the OmcA protein, using atomistic molecular dynamics simulations. Our study shows that NP interactions with the OM are primarily electrostatic, while the stability of the MtrCAB complex within the lipid layers depends on both hydrophobic and electrostatic forces. The NP interacts more strongly with the MtrCAB protein complex and lipid layer simultaneously than with either component alone when the steric effect of LPS is not considered. On the extracellular side of MtrC, the NP adsorbs most strongly to outward-facing sites, particularly near the terminal regions (hemes 2 and 10, and hemes 4 and 5) of the staggered heme network. The NP adsorption on the lipid membrane leads to surface diffusion and to binding with the MtrCAB complex without altering its secondary structure, while internalization is prevented due to strong hydration of the NP surface. It also induces orientational shifts of the protein complex, which depend on the specific MtrCAB subunit contacting the NP. A comparison of edge-to-edge heme distances between NP-bound and unbound structures shows that NP adsorption perturbs the heme network in a nonlocal manner. The structural robustness of the protein complex and lipid membrane, along with the alteration of the heme network upon NP adsorption, demonstrates the bacteria's adaptation to the environment.