Resilience, Dynamics, and Interactions within a Model Multispecies Exoelectrogenic-Biofilm Community

Abstract

Anode-associated multispecies exoelectrogenic biofilms are essential for the function of bioelectrochemical systems (BESs). The individual activities of anodeassociated organisms and physiological responses resulting from coculturing are often hard to assess due to the high microbial diversity in these systems. Therefore, we developed a model multispecies biofilm comprising three exoelectrogenic proteobacteria, Shewanella oneidensis, Geobacter sulfurreducens, and Geobacter metallireducens, with the aim to study in detail the biofilm formation dynamics, the interactions between the organisms, and the overall activity of an exoelectrogenic biofilm as a consequence of the applied anode potential. The experiments revealed that the organisms build a stable biofilm on an electrode surface that is rather resilient to changes in the redox potential of the anode. The community operated at maximum electron transfer rates at electrode potentials that were higher than 0.04 V versus a normal hydrogen electrode. Current densities decreased gradually with lower potentials and reached half-maximal values at Ϫ0.08 V. Transcriptomic results point toward a positive interaction among the individual strains. S. oneidensis and G. sulfurreducens upregulated their central metabolisms as a response to cultivation under mixed-species conditions. G. sulfurreducens was detected in the planktonic phase of the bioelectrochemical reactors in mixed-culture experiments but not when it was grown in the absence of the other two organisms.IMPORTANCE In many cases, multispecies communities can convert organic substrates into electric power more efficiently than axenic cultures, a phenomenon that remains unresolved. In this study, we aimed to elucidate the potential mutual effects of multispecies communities in bioelectrochemical systems to understand how microbes interact in the coculture anodic network and to improve the community's conversion efficiency for organic substrates into electrical energy. The results reveal positive interactions that might lead to accelerated electron transfer in mixedspecies anode communities. The observations made within this model biofilm might be applicable to a variety of nonaxenic systems in the field.KEYWORDS bioelectrochemical systems, Shewanella, Geobacter, exoelectrogenic biofilm, transcriptome analysis S everal microorganisms have the ability to transfer respiratory electrons to an extracellular electron acceptor. Extracellular respiration is highly relevant for a number of biogeochemical cycles, because these electron transport chains were developed for reducing metal oxides as well as for nonmembrane-permeable environmental electron shuttles, such as humic substances (1-4). It is likely that the selective pressure to evolve terminal reductases that catalyze electron transfer to solid electron

Flavin-mediated extracellular electron transfer in Gram-positive bacteria Bacillus cereus DIF1 and Rhodococcus ruber DIF2

“…Flavin molecules have been found as endogenous electron shuttles that can interact with the electron acceptor to promote ideal organism growth. 34 In our experiments, the FMN concentration increased aer the growth of bacterial cells to the log phase, which indicated that FMN plays an important role in extracellular electron transfer in the strain DIF1 and strain DIF2. This may also be shown by the current increase aer adding RF and FMN (Fig.…”

“…Shewanella species were also shown to secrete avins as electron mediators, but direct contactdependent electron transfer was still the main pattern of electron transfer. 14,24,25,32,34 In our experiment, when the anode with the biolm was placed into a fresh anolyte, the redox activity was fairly weak. When a new anode was immersed in the spent anolyte, the redox peaks were obvious, as shown in Fig.…”

Strategies for the Targeted Improvement of Anodic Electron Transfer in Microbial Fuel Cells

“…A biological approach comprises the genetic modification of electrochemically active microorganisms. The use of defined mixed cultures represents another option, because the electron transfer efficiency can be improved by mutual interactions between organisms , . In physico‐chemical approaches, the electrode surface and its interaction with the microorganisms as well as the application of redox mediators constitute a central aspect of this research .…”

“…They range from improved anaerobic conditions for electrogens due to oxygen depletion to their extended substrate accessibility or their simultaneous utilization of different EET types , . Additionally, the current density could be increased to a total of 6000–6400 mA m −2 by cocultivating G. sulfurreducens (generating a current density in the corresponding pure culture of 4700 mA m −2 ), Geobacter metallireducens (600 mA m −2 ) and S. oneidensis (1300 mA m −2 ), which has been associated with both the upregulation of the central metabolism and cytochrome‐related gene expression as well as the interorganismal use of secreted redox mediators . Further investigations confirmed the positive effect of defined mixed cultures of G. sulfurreducens and S. oneidensis on one another based on the 38 % higher current density (5400 ± 700 mA m −2 ) and 35 % thicker biofilm dominated by G. sulfurreducens (93 ± 8 µm) in comparison to the individual pure cultures ( G. sulfurreducens with 3900 ± 900 mA m −2 and S. oneidensis with 340 ± 11 mA m −2 ) .…”

Reduction of sulfur and oxidized forms of nitrogen by bacteria of Desulfuromonas sp., isolated from Yavorivske Lake, under the influence of ferrum citrate

“…Most representatives of sulfidogenic bacteria have a nonspecific metal reductase enzyme system that allows them to use compounds of Fe(III), Mn(IV), U(VI), Cr(VI), Cu(II) and other metals as electron acceptors of anaerobic respiration (Kozlova et al, 2008). Soluble and insoluble metal compounds are reduced outside the cells by a system of membrane-bound metal reductases (multi-heme c-type cytochromes) (Gescher & Kappler, 2012;Richter et al, 2012;Breuer et al, 2015), therefore electrons are released into the medium, allowing these exoelectrogenic anaerobic bacteria to be used in the microbial fuel cells (MFC) as the high effective anode biocatalysts (Fitzgerald et al, 2013;Prokhorova et al, 2017;Simonte et al, 2017). Electric current generation by Desulfuromonas acetoxidans IMV B-7384 in a MFC was described (Bilyy et al, 2014;Vasyliv et al, 2015), and the interrelation between Fe(III) reduction and exoelectrogenesis performed by this bacteria in the MFC was established (Vasyliv et al, 2016).…”