Electric field stimulates production of highly conductive microbial OmcZ nanowires

Abstract

Multifunctional living materials are attractive due to their powerful ability to self-repair and replicate. However, most natural materials lack electronic functionality. Here we show that an electric field, applied to electricity-producing Geobacter sulfurreducens biofilms, stimulates production of previously unknown cytochrome OmcZ nanowires with 1,000-fold higher conductivity (30 S/cm), and 3-fold higher stiffness (1.5 GPa), than the cytochrome OmcS nanowires that are important in natural environments. Using chemical imaging-based multimodal nanospectroscopy, we correlate protein structure with function, and observe pH-induced conformational switching to β-sheets in individual nanowires, which increases their stiffness and conductivity by 100-fold due to enhanced π-stacking of heme groups; this was further confirmed by computational modelling and bulk spectroscopic studies. These nanowires can transduce mechanical and chemical stimuli into electrical signals to perform sensing, synthesis and energy production. These findings of biologically-produced, highly-conductive protein nanowires may help to guide the development of seamless, bidirectional interfaces between biological and electronic systems.

Spatially Resolved Electron Transport through Anode‐Respiring Geobacter sulfurreducens Biofilms: Controls and Constraints

“…Moreover, the polymerization of monomeric cytochromes (e.g. OmcZ) could further reduce the heme-heme distance [33] . At such closely packed distance, multistep electron hopping along the conductive filaments thus are made possible (< 20 Å [26,27] ).…”

Bioelectrochemistry and the Singularity Point “I Robot”?**

“…Nikhil Malvankar and team [36] (Figure 1(A)) and Thomas Clarke together with Julea Butt and their teams have shown several structures of long‐range multi‐heme c‐type cytochromes pili like structures that span the cellular membranes and deliver electrons from the internal environment of cells to external electron acceptors with very high conductivity. The Mavlankar team has recently demonstrated the control of biofilms of G. sulforreducens conductivity through electrode potential bias, this report demonstrates and emphasizes even further both the role of porphyrins in the electrochemical properties of biofilms as well as the ability to manipulate biofilms’ properties and specifically their electrochemical properties using electrodes [37] . Based on these findings in natural pili, artificial pili like structures were designed and have shown conductivity in‐vitro (Figure 1(B)) [38] …”

“…The Mavlankar team has recently demonstrated the control of biofilms of G. sulforreducens conductivity through electrode potential bias, this report demonstrates and emphasizes even further both the role of porphyrins in the electrochemical properties of biofilms as well as the ability to manipulate biofilms' properties and specifically their electrochemical properties using electrodes. [37] Based on these findings in natural pili, artificial pili like structures were designed and have shown conductivity in-vitro ( Figure 1(B)). [38]…”

Geobacter sulfurreducensinner membrane cytochrome CbcBA controls electron transfer and growth yield near the energetic limit of respiration

“…may explain this flexibility, with multiple c-type cytochromes and extracellular appendages identified that facilitate reduction of extracellular compounds. In G. sulfurreducens, at least five triheme cytochromes are linked to periplasmic electron transfer [23,24], five multi-protein cytochrome complexes aid electron transfer through the outer membrane [25], and both multiheme cytochrome nanowires and extracellular pili extend beyond the cell [26,27,28]. Some outer membrane cytochromes are necessary for reduction of specific oxyanions such as SeO3 2− [29], or use of Fe(III) vs. electrode surfaces [25,30], but none explain how Geobacter might adapt its energy generation strategy to changes in redox potential.…”