Bio-nano hybrids: molecular interactions between iron oxide nanoparticles and outer-membrane extracellular cytochromes of Shewanella oneidensis

Metal oxide nanoparticles (NPs) coupled with dissimilatory metal-reducing bacteria enable continuous redox cycling through extracellular electron transfer (ET), a process central to bioremediation and bioenergy applications. However, the molecular mechanisms governing ET at the outer membrane-iron oxide NP interface remain unclear. Here, atomistic molecular dynamics simulations were employed to elucidate how the extracellular cytochromes of Shewanella oneidensis cooperatively mediate iron oxide NP adsorption, a prerequisite for extracellular ET. Our study shows that MtrF and two OmcA decaheme cytochromes are asymmetrically associated through their N- and C-terminal regions with distinct interaction energies, and their terminal heme groups (heme 10) of the long chains in the staggered cross-heme networks are connected to form a continuous heme network. This assembly sterically occludes MtrF heme 10 and redirects NP adsorption to alternative termini of the cross-heme network, including heme 5 (the opposite end of the long heme chain), where MtrF mediates binding through electrostatic interactions involving its heme groups and surface residues. NP adsorption also occurs near heme 2 at the terminus of the MtrF short heme chain, where OmcA residues primarily stabilize NP attachment. These results identify MtrF as the primary mediator of extracellular ET and establish OmcA as an interfacial stabilizer that enhances NP binding without directly mediating ET.