A biophotoelectrochemical approach to unravelling the role of cyanobacterial cell structures in exoelectrogenesis

Abstract

Photosynthetic microorganisms can export electrons outside their cells, a phenomenon called exoelectrogenesis, which can be harnessed for solar energy conversion. However, the route electrons take from thylakoid membranes to the cell exterior is not understood. Electrochemistry is a powerful analytical technique for studying electron transfer pathways. Here, we show how photoelectrochemistry can be used to compare electron flux from cyanobacterial cells of different growth stages, species and with the outer layers systematically removed. We show that the periplasmic space contributes significantly to the photocurrent profile complexity of whole cells, indicating that it gates electron transfer in exoelectrogenesis. We found that although components of the type IV pili machinery do not have a role in exoelectrogenesis, they contribute significantly to cell-electrode adherence. This study establishes that analytical photoelectrochemistry and molecular microbiology provide a powerful combination to study exoelectrogenesis, enabling future studies to answer biological questions and advance solar energy conversion applications.

Green notes: The rhythms of cyanobacteria exoelectrogenesis as de-composed by the Hilbert-Huang transform

“…For example, Synechocystis is known to have lower amplitude and less accurate circadian rhythms than S. elongatus 28 . This is consistent with higher peaks and troughs reported in Synechococcus chronoamperograms 8 . Finally, a confirmation of the hypotheses developed in this work may offer a bioelectrochemical approach for performing simple chronobiology experiments that eliminates the need for engineering reporter strains and extensive fluorescence measurements typical in the study of cyanobacteria circadian rhythms, while increasing the time resolution of experiments.…”

“…This remains a major hurdle in advancing the fundamental understanding needed to develop more efficient light conversion, and to enable applied research to realise the technology at a commercial scale. To date, electron flows have been primarily investigated via spectroscopy and electrochemical techniques such as chronoamperometry and cyclic voltammetry studies on mutant, stressed or inhibited cells [2][3][4][5][6][7][8] . Computational models and tools are being developed that can be used to help interpret experimental data and run rapid simulations towards understanding the electron flows [9][10][11] .…”

Living electronics: A catalogue of engineered living electronic components

“…In addition to pursuing a better mechanistic understanding of the EET pathways in photosynthetic microbes, the field of biophotovoltaics has focused on optimizing these systems (Wey et al, 2019 ). This work has included enhancing biofilm formation (Wey et al, 2021 ), creating porous electrodes with increased surface area (Wenzel et al, 2018 ; Zhang et al, 2018 ), disrupting the cell surface (Kusama et al, 2022 ; Saper et al, 2018 ; Wey et al, 2021 ), introducing additional redox‐active molecules (Clifford et al, 2021 ) or EET proteins (Meng et al, 2021 ; Schuergers et al, 2017 ; Sekar et al, 2016 ) and creating microbial consortia where photosynthetic microbes use light to produce electron donor chemicals that other electroactive microbes can use to produce current (Zhu et al, 2019 ). Biophotovoltaic devices using Synechocystis have proven functional as continuous power sources for low‐powered electronics such as a digital clock (McCormick et al, 2011 ) and a microprocessor (Bombelli et al, 2022 ).…”