Addition of Riboflavin-Coupled Magnetic Beads Increases Current Production in Bioelectrochemical Systems via the Increased Formation of Anode-Biofilms.

Tutut Arinda,Markus Stöckl,Miriam Edel,David Rehnlund,Roland Ulber,Dirk Holtmann,Johannes Gescher,Laura-Alina Philipp,Katrin Sturm-Richter,Jonas Chodorski

doi:10.3389/fmicb.2019.00126

Abstract

Shewanella oneidensis is one of the best-understood model organisms for extracellular electron transfer. Endogenously produced and exported flavin molecules seem to play an important role in this process and mediate the connection between respiratory enzymes on the cell surface and the insoluble substrate by acting as electron shuttle and cytochrome-bound cofactor. Consequently, the addition of riboflavin to a bioelectrochemical system (BES) containing S. oneidensis cells as biocatalyst leads to a strong current increase. Still, an external application of riboflavin to increase current production in continuously operating BESs does not seem to be applicable due to the constant washout of the soluble flavin compound. In this study, we developed a recyclable electron shuttle to overcome the limitation of mediator addition to BES. Riboflavin was coupled to magnetic beads that can easily be recycled from the medium. The effect on current production and cell distribution in a BES as well as the recovery rate and the stability of the beads was investigated. The addition of synthesized beads leads to a more than twofold higher current production, which was likely caused by increased biofilm production. Moreover, 90% of the flavin-coupled beads could be recovered from the BESs using a magnetic separator.

Highlights

In microbial fuel cells, microorganisms catalyze the direct conversion of chemical energy into an electrical current
A low riboflavin concentration on current production in a bioelectrochemical system (BES) inoculated with MR-1 was tested first
A 50-fold higher shuttle concentration resulted in a linear increase of the current density, but for economic reasons we chose 37 nM riboflavin as suitable working concentration for further experiments

Summary

Introduction

Microorganisms catalyze the direct conversion of chemical energy into an electrical current. The pathway of electron flow toward the extracellular space is similar in MR-1 and PCA (Shi et al, 2014) Both organisms are Gramnegative, which means that respiratory electrons are transported from the cytoplasmic membrane through the periplasm and across the outer membrane in order to be transferred onto insoluble electron acceptors like metals, iron minerals or an anode (Simonte et al, 2017; Beblawy et al, 2018; Costa et al, 2018). This includes either direct contact of enzymes and acceptor (White et al, 2016; Simonte et al, 2017), reduction via conductive extracellular appendages (so called nanowires) (Reguera et al, 2005; Gorby et al, 2006; Malvankar et al, 2011; Polizzi et al, 2012) or mediated transfer through the reduction of electron carriers [usually small, low-weight, soluble redox molecules (e.g., phenazine and quinones)] in a process termed electron shuttling (Lovley et al, 1998; Okamoto et al, 2015)

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