Potential regulates metabolism and extracellular respiration of electroactive Geobacter biofilm

Abstract

Dissimilatory metal reducer Geobacter sulfurreducens can mediate redox processes through extracellular electron transfer and exhibit potential‐dependent electrochemical activity in biofilm. Understanding the microbial acclimation to potential is of critical importance for developing robust electrochemically active biofilms and facilitating their environmental, geochemical, and energy applications. In this study, the metabolism and redox conduction behaviors of G. sulfurreducens biofilms developed at different potentials were explored. We found that electrochemical acclimation occurred at the initial hours of polarizing G. sulfurreducens cells to the potentials. Two mechanisms of acclimation were found, depending on the polarizing potential. In the mature biofilms, a low level of biosynthesis and a high level of catabolism were maintained at +0.2 V versus standard hydrogen electrode (SHE). The opposite results were observed at potentials higher than or equal to +0.4 V versus SHE. The potential also regulated the constitution of the electron transfer network by synthesizing more extracellular cytochrome c such as OmcS at 0.0 and +0.2 V and exhibited a better conductivity. These findings provide reasonable explanations for the mechanism governing the electrochemical respiration and activity in G. sulfurreducens biofilms.

Spatially Resolved Electron Transport through Anode‐Respiring Geobacter sulfurreducens Biofilms: Controls and Constraints

“…Indeed, an earlier study directly observed that redox potential decreases significantly with increasing distance from the anode surface [59] . In addition, earlier redox titration studies showed that G. sulfurreducens biofilms or cytochromes were predominantly reduced at lower potentials, [39,43,79] agreeing with our simulation result overall ( Figure S8E). However, those studies suggest that cytochrome would be substantially oxidized above +0.1V.…”

“…However, those studies suggest that cytochrome would be substantially oxidized above + 0.1 V. The difference between the experimental observations and our simulations are likely attributed to the experimental procedure in which the cytochrome sample was purified [80,81] or that G. sulfurreducens cells were starved and no acetate was provided prior and during the electrochemical titration. [39,43] Finally, electron stored in reduced Cyt red can be recovered as current when the electric potential is sufficient to transport electrons toward electrode. [41,82] Assuming each Cyt red holds one electron, under our modeled conditions the stored electrons in Cyt red at steady state are estimated to be~1.84-1.99 × 10 À 18 mol e À cell À 1 and 0.8-3.4 × 10 À 18 mol e À cell À 1 at high and low anode potential setting respectively, with more stored electrons in Cyt red at the biofilm surface.…”

“…[34][35][36][37][38][39][40][41][42] The anode potential regulates metabolism, electrochemical respiration and anabolic activity in G. sulfurreducens biofilms. [43][44][45][46] Understanding how G. sulfurreducens produces high current densities, and what ultimately is responsible for limiting this process motivates the development of a reactive transport model. Such models account for the fundamental physics and chemistry in natural systems and can quantitatively integrate microbiological insights into an environmental context.…”

“…Korth and Harnisch (2019) [52] recently presented a model of direct EET that demonstrates that energy harvest not only depends on anode potential but can be determined by intracellular conditions. Thus, earlier studies showed that both pH [53][54][55] and electric potential dependencies [42][43][44][45][46]56,57] shape cell activity within biofilms. However, until recently, no robust, direct, and spatially resolved cell activity data was available.…”

Microbial electrolysis cell (MEC): Strengths, weaknesses and research needs from electrochemical engineering standpoint

“…How can it be forced to form the most electron conductive matrix [145][146][147][148]? The applied potential may be a tool that helps to achieve this objective [149,150] but may not always be effective [151,152]. This item is still under debate [153,154,101] (see a short review in [114]).…”