Long-distance electron transfer in a filamentous Gram-positive bacterium

Yonggang Yang,Jean Manca,Guoping Sun,Chunjie Zhu,Jesper Tataru Bjerg,Cuifen Gan,Jun Guo,Meiying Xu,Robin Bonné,Yuxin Ma,Guannan Kong,Mingdong Dong,Lasse Hyldgaard Klausen,Dizhou Luo,Lars Peter Nielsen,Mathijs Meert,Zegao Wang

doi:10.1038/s41467-021-21709-z

Abstract

Long-distance extracellular electron transfer has been observed in Gram-negative bacteria and plays roles in both natural and engineering processes. The electron transfer can be mediated by conductive protein appendages (in short unicellular bacteria such as Geobacter species) or by conductive cell envelopes (in filamentous multicellular cable bacteria). Here we show that Lysinibacillus varians GY32, a filamentous unicellular Gram-positive bacterium, is capable of bidirectional extracellular electron transfer. In microbial fuel cells, L. varians can form centimetre-range conductive cellular networks and, when grown on graphite electrodes, the cells can reach a remarkable length of 1.08 mm. Atomic force microscopy and microelectrode analyses suggest that the conductivity is linked to pili-like protein appendages. Our results show that long-distance electron transfer is not limited to Gram-negative bacteria.

Highlights

Long-distance extracellular electron transfer has been observed in Gram-negative bacteria and plays roles in both natural and engineering processes
Two bacterial long-distance electron transfer (LDET) strategies have been identified: conductive protein nanowires generated by relatively short, unicellular bacteria (e.g., Geobacter species) and conductive envelopes formed by filamentous, multicellular cable bacteria[4,8]
We found that GY32 could grow into a longer shape when anaerobically respiring with graphite electrodes as the sole electron acceptor in microbial fuel cells (MFCs) (Fig. 1a and Supplementary Fig. 1)

Summary

Introduction

Long-distance extracellular electron transfer has been observed in Gram-negative bacteria and plays roles in both natural and engineering processes. The electron transfer can be mediated by conductive protein appendages (in short unicellular bacteria such as Geobacter species) or by conductive cell envelopes (in filamentous multicellular cable bacteria). Some single-celled bacteria are capable of long-distance electron transfer (LDET) to chemicals or other microbial cells at tens of micrometers distance[4,5,6] and multicellular cable bacteria transport electrons in the range of centimetres[7,8]. Two bacterial LDET strategies have been identified: conductive protein nanowires generated by relatively short, unicellular bacteria (e.g., Geobacter species) and conductive envelopes formed by filamentous, multicellular cable bacteria[4,8]. In microbial fuel cells (MFCs) strain GY32 can form centimetre-range conductive cellular networks composed of insulated filamentous cells with conductive nanowire-like appendages

Methods

Results

Conclusion