Core/Shell Bacterial Cables: A One-Dimensional Platform for Probing Microbial Electron Transfer.

Abstract

Extracellular electron transfer (EET) from electrochemically active bacteria (EAB) plays a critical role in renewable bioelectricity harvesting through microbial fuel cells (MFC). Comprehensive interpretation and interrogation of EET mechanisms can provide valuable information to enhance MFC performance, which however are still restricted by the intrinsic complexity of natural biofilm. Here, we design core/shell EAB-encapsulating cables as a one-dimensional model system to facilitate EET studies, where the local microenvironments can be rationally controlled to establish structure-function correlations with full biological relevance. In particular, our proof-of-concept studies with Shewanella loihica PV-4 ( S. loihica) encapsulating cables demonstrate the precise modulation of fiber diameters (from 6.9 ± 1.1 to 25.1 ± 2.4 μm) and bacteria interactions, which are found to play important roles in programming the formation of different intercellular structures as revealed by in situ optical and ex situ electron microscopic studies. As-formed bacterial cables exhibit conductivity in the range of 2.5-16.2 mS·cm-1, which is highly dependent on the bacteria density as well as the nature and number of intercellular interconnections. Under electron-acceptor limited conditions, the closely contacted bacteria promote the development of high density self-assembling nanomaterials at cellular interfaces which can be directly translated to the increase of EET efficiency (16.2 mS·cm-1) as compared with isolated, remotely connected bacteria samples (6.4 mS·cm-1). Introducing exceeding concentrations of soluble electron acceptors during cell culture, however, substantially suppresses the formation of cellular interconnections and leads to significantly reduced conductivity (2.5 mS·cm-1). Frequency-dependent measurements further revealthat EET of EAB networks share similar characteristics to electron hopping in conductive polymer matrix, including dominant direct current-conduction in the low frequency region, and alternating current-induced additional electron hopping when the applied frequency is above the critical frequency (105 Hz). The current work represents a strategically new approach for noninvasively probing EET with rationally defined microenvironment and cellular interactions across a wide range of length scales, which is expected to open up new opportunities for tackling the fundamentals and implications of EET.