Type IV Pili-Independent Photocurrent Production by the Cyanobacterium Synechocystis sp. PCC 6803.

Miyuki A Thirumurthy,Anne K Jones,Andrew Hitchcock,Marko S Chavez,John T Heap,Jiawei Liu,Robert Ros,Bryant L Doss,Mohamed Y El-Naggar,Angelo Cereda,Thomas S Bibby

doi:10.3389/fmicb.2020.01344

Abstract

Biophotovoltaic devices utilize photosynthetic organisms such as the model cyanobacterium Synechocystis sp. PCC 6803 (Synechocystis) to generate current for power or hydrogen production from light. These devices have been improved by both architecture engineering and genetic engineering of the phototrophic organism. However, genetic approaches are limited by lack of understanding of cellular mechanisms of electron transfer from internal metabolism to the cell exterior. Type IV pili have been implicated in extracellular electron transfer (EET) in some species of heterotrophic bacteria. Furthermore, conductive cell surface filaments have been reported for cyanobacteria, including Synechocystis. However, it remains unclear whether these filaments are type IV pili and whether they are involved in EET. Herein, a mediatorless electrochemical setup is used to compare the electrogenic output of wild-type Synechocystis to that of a ΔpilD mutant that cannot produce type IV pili. No differences in photocurrent, i.e., current in response to illumination, are detectable. Furthermore, measurements of individual pili using conductive atomic force microscopy indicate these structures are not conductive. These results suggest that pili are not required for EET by Synechocystis, supporting a role for shuttling of electrons via soluble redox mediators or direct interactions between the cell surface and extracellular substrates.

Highlights

Electron transfer and redox reactions form the foundation for energy transduction in biological systems (Marcus and Sutin, 1985)
The latter has been proposed to proceed via redox proteins on the cell surface or via extracellular appendages that have come to be known as bacterial nanowires (Gorby et al, 2006; El-Naggar et al, 2010)
The composition of these nanowires is hypothesized to vary between different organisms; recent work by El-Naggar and coworkers has shown that the nanowires of Shewanella oneidensis MR-1 are extensions of electron transfer (EET)-protein-containing outer membrane that appear to form from chains of vesicles (Pirbadian et al, 2014)

Summary

Introduction

Electron transfer and redox reactions form the foundation for energy transduction in biological systems (Marcus and Sutin, 1985). Two distinct mechanisms have been hypothesized to account for extracellular electron transfer (EET) in anaerobic, heterotrophic bacteria: utilization of soluble, diffusing redox shuttles like flavins to transfer electrons from the cellular interior to the extracellular surface (Watanabe et al, 2009; Glasser et al, 2017) and direct interaction between a redox-active component on the cell surface and the extracellular target (Shi et al, 2009) The latter has been proposed to proceed via redox proteins on the cell surface (e.g., multiheme cytochromes) or via extracellular appendages that have come to be known as bacterial nanowires (Gorby et al, 2006; El-Naggar et al, 2010). Details about the types of charge carriers and the exact mechanisms of interfacial electron transport within conductive appendages remain unclear

Methods

Results

Conclusion