Electrochemically active bacteria sense electrode potentials for regulating catabolic pathways

Hirose, Atsumi; Kasai, Takuya; Aoki, Motohide; Umemura, Tomonari; Watanabe, Kazuya; Kouzuma, Atsushi

doi:10.1038/s41467-018-03416-4

Cited by 119 publications

(91 citation statements)

References 70 publications

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“…One conceivable assumption is that the redox state of proteins or quinones in the respiration system of G. sulfurreducens may be sensed and makes a feedback to processes such as the TCA cycle. Recently, the Arc system has been shown to sense the potential and regulate the intracellular metabolism in Shewanella oneidensis MR‐1 (Hirose et al, ). It is possible that G. sulfurreducens possesses similar systems for sensing the potential and regulating biosynthesis and the catabolism.…”

Section: Resultsmentioning

confidence: 99%

Potential regulates metabolism and extracellular respiration of electroactive Geobacter biofilm

Liu

et al. 2019

Biotech & Bioengineering

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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.

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Section: Resultsmentioning

confidence: 99%

Potential regulates metabolism and extracellular respiration of electroactive Geobacter biofilm

Liu

et al. 2019

Biotech & Bioengineering

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“…Recent results indicate that the redox potential of the terminal electron acceptor influences the percentage to which the NADH‐ and formate‐dehydrogenases contribute to the reduction of the quinone pool. Using a bioelectrochemical system and a working electrode poised to either +0.5 V, +0.2 V or 0 V vs. SHE ( S tandard H ydrogen E lectrode), Hirose and colleagues could elucidate that a deletion mutant in all four NADH dehydrogenase encoding gene clusters is almost completely unable to produce current at +0.5 V (Hirose et al, ). In contrary, the difference in current production was not significant compared to the wild type at the lower potentials tested.…”

Section: Introductionmentioning

confidence: 99%

Extracellular reduction of solid electron acceptors byShewanella oneidensis

Beblawy

Bursac

Paquete

et al. 2018

Molecular Microbiology

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Shewanella oneidensis is the best understood model organism for the study of dissimilatory iron reduction. This review focuses on the current state of our knowledge regarding this extracellular respiratory process and highlights its physiologic, regulatory and biochemical requirements. It seems that we have widely understood how respiratory electrons can reach the cell surface and what the minimal set of electron transport proteins to the cell surface is. Nevertheless, even after decades of work in different research groups around the globe there are still several important questions that were not answered yet. In particular, the physiology of this organism, the possible evolutionary benefit of some responses to anoxic conditions, as well as the exact mechanism of electron transfer onto solid electron acceptors are yet to be addressed. The elucidation of these questions will be a great challenge for future work and important for the application of extracellular respiration in biotechnological processes.

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“…To overcome the hurdle of electron transfer across 13 the otherwise electrically-insulating cell envelope, these bacteria rely on a number of mechanisms: 14 multiheme cytochrome complexes that bridge the periplasm and outer membrane (10)(11)(12), microbial 15 nanowires that reach out to distant electron acceptors (13,14), and soluble redox shuttles that diffusively 16 link cells to external surfaces (15,16). EET can be electrochemically mimicked on electrode surfaces that 17 function as surrogate electron acceptors (anodes) or donors (cathodes) to support microbial metabolism, 18 depending on the poised potentials of these electrodes (17)(18)(19)(20)(21)(22). As a result, electrochemical enrichments 19 have been applied to microbial samples from a variety of environments (23)(24)(25)(26)(27)(28)(29)(30)(31).…”

Section: Introductionmentioning

confidence: 99%

“…As a result, electrochemical enrichments 19 have been applied to microbial samples from a variety of environments (23)(24)(25)(26)(27)(28)(29)(30)(31). When combined with 20 surveys of microbial community structure, these electrochemical techniques greatly expanded our 21 understanding of the phylogenetic diversity of microbes capable of colonizing electrodes and led to the 22 isolation of novel microorganisms capable of EET to anodes (32)(33)(34)(35)(36)(37). While our mechanistic understanding 23 of the molecular pathways that underlie inward EET (i.e., electron transfer from rather than to surfaces) 24 5 lags behind metal reduction pathways, electrode-based techniques have highlighted the diversity of 1 microbes capable of electron uptake from cathodes: acetogens, methanogens, as well as iron-and sulfur-2 oxidizers (38)(39)(40)(41)(42)(43)(44)(45).…”

Section: Introductionmentioning

confidence: 99%

“…16 Here we report the deployment and operation of an in situ electrochemical colonization (ISEC) 17 reactor fed by a manifold at the 4850 ft (1478 m) level of SURF. The reactor contained four working 18 electrodes, poised at potentials spanning reducing/cathodic to oxidizing/anodic, to act as an inexhaustible 19 source or sink of electrons for capture of potential mineral oxidizing and reducing bacteria, with emphasis 20 on mimicking sulfur oxidation, iron oxidation, and manganese reduction predicted as energy-yielding 21 reactions in this manifold (50). Our goals were twofold: 1) to demonstrate the use of electrodes as in situ 22 observatories for directly detecting and characterizing microbial electron transfer activity, and 2) to capture 23 important bacterial lineages active in the deep subsurface.…”

Section: Introductionmentioning

confidence: 99%

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In Situ Electrochemical Studies of the Terrestrial Deep Subsurface Biosphere at the Sanford Underground Research Facility, South Dakota, USA

Jangir

Karbelkar

Beedle

et al. 2019

Preprint

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250 words) 1 The terrestrial deep subsurface is host to significant and diverse microbial populations. However, these 2 microbial populations remain poorly characterized, partially due to the inherent difficulty of sampling, in 3 situ studies, and isolating of the in situ microbes. Motivated by the ability of microbes to gain energy from 4 redox reactions at mineral interfaces, we here present in situ electrochemical colonization (ISEC) as a 5 method to directly study microbial electron transfer activity and to enable the capture and isolation of 6 electrochemically active microbes. We installed a potentiostatically controlled ISEC reactor containing four 7 working electrodes 1500 m below the surface at the Sanford Underground Research Facility. The working 8 electrodes were poised at different redox potentials, spanning anodic to cathodic, to mimic energy-yielding 9 mineral reducing and oxidizing reactions predicted to occur at this site. We present a 16S rRNA analysis 10 of the in situ electrode-associated microbial communities, revealing the dominance of novel bacterial 11 lineages under cathodic conditions. We also demonstrate that the in situ electrodes can be further used for 12 downstream electrochemical laboratory enrichment and isolation of novel strains. Using this workflow, we 13 isolated Bacillus, Anaerospora, Comamonas, Cupriavidus, and Azonexus strains from the electrode-14 attached biomass. Finally, the extracellular electron transfer activity of the electrode-oxidizing Comamonas 15 strain (isolated at -0.19 V vs. SHE and designated WE1-1D1) and the electrode-reducing Bacillus strain 16 (isolated at +0.53 V vs. SHE and designated WE4-1A1-BC) were confirmed in electrochemical reactors. 17 Our study highlights the utility of in situ electrodes and electrochemical enrichment workflows to shed light 18 on microbial activity in the deep terrestrial subsurface. 19

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Electrochemically active bacteria sense electrode potentials for regulating catabolic pathways

Cited by 119 publications

References 70 publications

Potential regulates metabolism and extracellular respiration of electroactive Geobacter biofilm

Potential regulates metabolism and extracellular respiration of electroactive Geobacter biofilm

Extracellular reduction of solid electron acceptors byShewanella oneidensis

In Situ Electrochemical Studies of the Terrestrial Deep Subsurface Biosphere at the Sanford Underground Research Facility, South Dakota, USA

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