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Background
Bioelectrochemical system (BES) has gained increased attention due to their versatile functions in energy pro- duction, environmental remediation, electrosynthe- sis, and remoting sensing [1–3]. Microbial extracellular electron transfer (EET) is essential in driving the micro- bial interspecies interaction and redox reactions in both natural and engineered environments. Three types of EET pathways were identified: outer-membrane c-type cytochromes, conductive pili, and electron shuttles [4– 6], and recent studies found an additional EET pathway mediated by conductive minerals [7]. For instance, mag- netite (Fe3O4) is a conductive mineral that can be used as electron conduits to facilitate EET of Fe(III)-reducing microorganisms. This also compensates for the lack of OmcS to mediate electron transfer between the pili of Geobacter sulfurreducens and electron donors or accep- tors [8, 9]. Furthermore, electrically conductive mag- netite nanoparticles are able to facilitate interspecies electron transfer (IET) between Geobacter sulfurreducens and Thiobacillus denitrificans, which in turn are able to establish a cooperative metabolism [10]. Nowadays, mag- netite has been used for a wide range of applications due to its superparamagnetic properties, low mass transfer resistance, and selective separation of immobilized bio- molecules and bacteria by applying magnetic fields (MFs) [11, 12].
Magnetic fields (MFs) provide a cost-effective and convenient approach in changing microbial activity. It has been used in various kinds of MFs-assisted bioreac- tors [13–15]. Earlier studies demonstrated that MF was able to promote the biocatalytic processes mediated by cytochrome c and to enhance electrical output of the biofuel cells through the magnetohydrodynamics [13, 16]. Recent studies showed that electricity production by MFCs was improved significantly by a static MF [17, 18]. The removal of chemical oxygen demand (COD) in wastewater treatment increases when MFs are applied on MFCs [19]. MFs enhanced bioelectrochemical activi- ties of anodic biofilms, while there was no increase in secretion of redox mediators [20]. Previous studies have shown that MFs enhanced the performance of MFCs. No investigation on how magnetite and MFs influence microbial community structures in MFCs that affect EET. Compared with the permanent magnet, the electromag- netic devices with adjustable intensity and direction of magnetic fields can provide use flexibility for the large- scale BESs. However, the effect of pulse electromagnetic field (PEMF) on BESs has not been investigated.
Electrodes modified with metal oxide, conducting polymer, and nanocomposite have been studied in order to enhance EET and enrichment of exoelectrogenic bac- teria [21–26]. However, magnetic material-modified
electrodes have not been applied in BESs. Some proper- ties of magnetite (Fe3O4) are sensitive to oxidation, and agglomeration and low conductivity makes it less than ideal. To circumvent this, Fe3O4 has been used as hybrid material with various other materials that enhances the properties of the magnetic particles. Polyaniline (PANI) is a carbon–nitrogen precursor that is popular within carbon material preparation because they have an aro- matic structure that is conductive to the formation of graphitization structure after carbonization, and it was shown to improve the performance of MFCs as the con- ductive polymer [27–29] by serving as a conductive and protective shell for magnetite in Fe3O4/polyaniline hybrid [12, 30, 31].
In this study, we hypothesized that the magnetic car- bon particle-modified electrodes in BESs may facilitate EET and current production under pulsed magnetic fields. To test this hypothesis, we constructed a new mag- netic bioelectrochemical system (MBES) with magnetic carbon particle-modified electrodes, and we developed a pulse electromagnetic field (PEMF) to hopefully enhance microbial extracellular electron transfer. Furthermore, we used molecular biology tools to understand the changes of microbial communities and interactions on the anode in response to PEMF operation in the PEMF-MBES reactors.
Methods
Synthesis of Fe3O4@N‐mC composite
The fabrication of Fe3O4@N-mC is previously described (Additional file 1: Fig. S1) [31]. Fe3O4@N-mC was the product of the carbonization of magnetic mesoporous polyaniline composite (Fe3O4@mPANI), and the Fe3O4@mPANI was obtained from aniline polymeriza- tion on the surface of the PVP-modified Fe3O4 particles (Fe3O4-PVP). Fe3O4-PVP was synthesized using the sol- vothermal method [32]. Ferric chloride hexahydrate, sodium acetate, and PVP were dissolved in ethylene glycol, and then crystallized at 200 °C for 8 h. Synthe- sized Fe3O4-PVP (black magnetic particles) was sepa- rated and recovered using a strong magnet. Fe3O4-PVP was added to the mixture of tergitol(tm)xh(nonionic) (P123) and sodium dodecyl sulfate (SDS) and dissolved in diluted hydrochloric acid (1 mol/L). After 30 min, it was ultrasonically dispersed, and the mixture was placed at 4 °C. The mixture was stirred, and aniline (0.1 mol/L) and ammonium persulfate (0.4 mol/L) were slowly added into the mixture. After that, the mixture was stirred for an additional 6 h to obtain Fe3O4@ mPANI. Finally, the Fe3O4@mPANI was carbonized with nitrogen at a heating rate of 3 °C min−1 to 700 °C and kept at 700 °C for 6 h in a tube furnace to synthe- sizeFe3O4@N-mC.
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