Electricity-driven metabolic shift through direct electron uptake by electroactive heterotroph Clostridiumpasteurianum

Abstract

Although microbes directly accepting electrons from a cathode have been applied for CO2 reduction to produce multicarbon-compounds, a high electron demand and low product concentration are critical limitations. Alternatively, the utilization of electrons as a co-reducing power during fermentation has been attempted, but there must be exogenous mediators due to the lack of an electroactive heterotroph. Here, we show that Clostridium pasteurianum DSM 525 simultaneously utilizes both cathode and substrate as electron donors through direct electron transfer. In a cathode compartment poised at +0.045 V vs. SHE, a metabolic shift in C. pasteurianum occurs toward NADH-consuming metabolite production such as butanol from glucose (20% shift in terms of NADH consumption) and 1,3-propandiol from glycerol (21% shift in terms of NADH consumption). Notably, a small amount of electron uptake significantly induces NADH-consuming pathways over the stoichiometric contribution of the electrons as reducing equivalents. Our results demonstrate a previously unknown electroactivity and metabolic shift in the biochemical-producing heterotroph, opening up the possibility of efficient and enhanced production of electron-dense metabolites using electricity.

Electro-Fermentation in Aid of Bioenergy and Biopolymers

“…In addition, while working with Geobacter sulfurreducens, it was observed that the fermentation pattern, as well as the microbial population could be influenced by EFs. A similar observation was made with C. pasteurianum that showed 21% shift in NADH-consumption to produce PDO using glycerol as substrate [79]. Such study increases the possibilities of efficient production of electron dense compounds using small quantities of electricity.…”

“…There are plenty of microbes possessing the ability to bioconvert glycerol into PDO. The recent advancements in cathodic EFs have led to enhanced PDO yield with the following advantages: (i) direct electron dissipation into PDO synthesis; (ii) selection of bacterial population adapted to reduced condition; and (iii) enhancing PDO generation as a sole NADH dissipating pathway [79]. Few studies have been performed on mixed culture glycerol EF using the strong negative potential of −1.14 V to achieve PDO production of 0.50 mol/mol glycerol, which is 2-fold higher than batch fermentation [80,81].…”

“…This leads to 61% enhancement in the overall ethanol yield, increasing the potential negatively influences the process [101]. Similarly, C. pasteurianum under electrochemical system displayed a shift in the metabolic pathway for enhanced production of butanol [79]. Besides glucose, other substrates such as acetate, glycerol, CO 2 , butyrate, etc.…”

“…Besides glucose, other substrates such as acetate, glycerol, CO 2 , butyrate, etc. have also been used for alcohol production [66,79]. A wild-type strain of C. pasteurianum was able to accept electrons from cathode during heterotrophic growth on glucose as well as glycerol leading to NADH-consuming compounds such as butanol and PDO [79].…”

Understanding extracellular electron transport of industrial microorganisms and optimization for production application

“…Both products present NADH sinks (see Figure 24) and therefore one could speculate that cathodic electron feed results in an increase of cellular NADH levels as seen for C. pasteurianum. 298 However, Therefore, all three mediators should provide electrons at a potential low enough to feed into the cellular NADH pool (around -280 mV required, refer to the discussion in section 4.1.5). As discussed above the redox-pools of C. autoethanogenum depend on ferredoxin, H 2 , NADH and NADPH.…”