Microbial electron transport and energy conservation - the foundation for optimizing bioelectrochemical systems

Abstract

Microbial electrochemical techniques describe a variety of emerging technologies that use electrode-bacteria interactions for biotechnology applications including the production of electricity, waste and wastewater treatment, bioremediation and the production of valuable products. Central in each application is the ability of the microbial catalyst to interact with external electron acceptors and/or donors and its metabolic properties that enable the combination of electron transport and carbon metabolism. And here also lies the key challenge. A wide range of microbes has been discovered to be able to exchange electrons with solid surfaces or mediators but only a few have been studied in depth. Especially electron transfer mechanisms from cathodes towards the microbial organism are poorly understood but are essential for many applications such as microbial electrosynthesis. We analyze the different electron transport chains that nature offers for organisms such as metal respiring bacteria and acetogens, but also standard biotechnological organisms currently used in bio-production. Special focus lies on the essential connection of redox and energy metabolism, which is often ignored when studying bioelectrochemical systems. The possibility of extracellular electron exchange at different points in each organism is discussed regarding required redox potentials and effect on cellular redox and energy levels. Key compounds such as electron carriers (e.g., cytochromes, ferredoxin, quinones, flavins) are identified and analyzed regarding their possible role in electrode-microbe interactions. This work summarizes our current knowledge on electron transport processes and uses a theoretical approach to predict the impact of different modes of transfer on the energy metabolism. As such it adds an important piece of fundamental understanding of microbial electron transport possibilities to the research community and will help to optimize and advance bioelectrochemical techniques.

Keywords: ATP yield; acetogenic bacteria; bio electrochemistry; bioelectrochemical system; microbial electron transport; microbial electrosynthesis; microbial fuel cell; redox potential.

FIGURE 1

Schematic image of the proposed EET of two metal respiring bacteria and their interactions with an electrode in a bioelectrochemical system. Dashed arrows indicate hypothetical electron flow and solid arrows indicate experimental proved electron flow. (A) Branched outer membrane cytochromes (OMCs) system of Geobacter sulfurreducens. Electrons can be transported between inner membrane, periplasm, outer membrane, and an electrode via a chain of cytochromes and menaquinones (MQ). Terminal OMCs can vary depending on the environmental conditions. (B) Unique Mtr-pathway and terminal reductases of Shewanella oneidensis. Quinones (Q) pass electrons to CymA or TorC, which transfer the electrons to terminal reductases or a MtrCAB complex. MtrCAB complex can interact with the electrode direct or via flavin molecules (FL).

FIGURE 2

Schematic image of acetogenic electron transport chains and possible interactions with an electrode in a bioelectrochemical system. Dashed arrows indicate hypothetical electron and proton flow. (A) Electron transport mechanisms in Moorella thermoacetica via membrane-bound cytochromes and hydrogenases, MQ, soluble electron-bifurcating complexes (Hyd and Nfn) and proton pumping Ech-complex; (B) Electron transport of Clostridium ljungdahlii (H⁺) and Acetobacterium woodii (Na⁺) based on membrane-bound Rnf-complex and soluble electron-bifurcating complexes (^∗Nfn-complex is not found in A. woodii). ? represents hypothetical cell-wall associated proteins that could facilitate electron transfer.

FIGURE 3

Redox potentials of important redox reactions in electron transport chains catalyzed by the bacteria discussed in this study. Standard redox potential (E^0′ [mV, 25°C, pH = 7]) are indicated by dashed lines. If physiological or environmental conditions are known to shift the potential from the E^0′, redox windows are indicated (solid lines). The bacterial symbol behind each reaction shows the organisms that are known to catalyze the reaction naturally. Blue: aerobes; green: facultative anaerobes; red–yellow: obligate anaerobes; Phenazine1 = Phenazine-1-carboxylic acid; Phenazine2 = Phenazine-1-carboxamide. ^∗c-type cytochromes can cover a broad range of redox potentials as indicated. Not all bacteria mentioned will cover the whole range. For detailed discussion refer to main text.

FIGURE 4

Schematic image of electron transport chains in Escherichia coli. NADH as electron donor via NADH dehydrogenase (NuoA-N), ubiquinone pool (UQ), succinate-dehydrogenase, and cytochromes bd (CydAB) and bo (CyoABCD). ATP is generated via F₁F₀-ATPase (3H⁺/ATP) from the membrane proton gradient. Possible sites of interaction with an electrode are indicated with dashed arrows. For detailed discussion and references refer to main text.