Outer membrane c-type cytochromes OmcA and MtrC play distinct roles in enhancing the attachment of Shewanella oneidensis MR-1 cells to goethite.

The outer membrane c-type cytochromes (c-Cyts) OmcA and MtrC in Shewanella are key terminal reductases that bind and transfer electrons directly to iron (hydr)oxides. Although the amount of OmcA and MtrC at the cell surface and their molecular structures are largely comparable, MtrC is known to play a more important role in dissimilatory iron reduction. To explore the roles of these outer membrane c-Cyts in the interaction of S. oneidensis MR-1 with iron oxides, the attachment processes of S. oneidensis MR-1 wild type and c-type cytochrome-deficient mutants (ΔomcA, ΔmtrC and ΔomcA-ΔmtrC) to goethite are compared via quartz crystal microbalance with dissipation monitoring (QCM-D). Strains with OmcA exhibit a rapid initial attachment. The quantitative model for QCM-D responses reveals that MtrC enhances the contact area and contact elasticity of cells with goethite by more than one and two times, respectively. In situ ATR-FTIR 2D-CoS analysis shows that MtrC promotes the initial interfacial reaction via an inner-sphere coordination. AFM analysis demonstrates that OmcA enhances the attractive force between cells and goethite by about 60%. As a result, OmcA contributes to higher attractive force with goethite and induces a rapid short-term attachment, while MtrC is more important in the longer-term interaction, through an enhanced contact area, which promotes interfacial reactions. These results reveal c-Cyts OmcA and MtrC adopt different mechanisms for enhancing the attachment of S. oneidensis MR-1 cells to goethite. It improves our understanding of the function of outer membrane c-Cyts and the influence of cell surface macromolecules in cell-mineral interactions.IMPORTANCE Shewanella species are one group of versatile and widespread dissimilatory iron-reducing bacteria, which are capable of respiring insoluble iron minerals via six multiheme c-type cytochromes. Outer membrane c-type cytochromes (c-Cyts) OmcA and MtrC are the terminal reductases in this pathway which share comparable protein structures. In this study, we elucidate the different roles of OmcA and MtrC in the interaction of S. oneidensis MR-1 with goethite at the whole-cell level. OmcA confers enhanced affinity towards goethite and results a rapid attachment. Meanwhile, MtrC increases the contact area of bacterial cells with goethite significantly and promotes the interfacial reaction which may explain its central role in extracellular electron transfer. This study provides novel insights into the role of bacterial surface macromolecules in the interfacial interaction of bacteria with minerals, which is critical to develop a comprehensive understanding of cell-mineral interactions.