scholarly journals Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis

mBio ◽  
2015 ◽  
Vol 6 (2) ◽  
Author(s):  
Jörg S. Deutzmann ◽  
Merve Sahin ◽  
Alfred M. Spormann
Keyword(s):  
Electron Transfer ◽  
Molecular Mechanisms ◽  
Solid Phase ◽  
Direct Electron Transfer ◽  
Extracellular Electron Transfer ◽  
Methane Formation ◽  
Electron Transfer Mechanism ◽  
Microbial Cells ◽  
Microbial Electrosynthesis ◽  
Microbially Influenced Corrosion

ABSTRACTDirect, mediator-free transfer of electrons between a microbial cell and a solid phase in its surrounding environment has been suggested to be a widespread and ecologically significant process. The high rates of microbial electron uptake observed during microbially influenced corrosion of iron [Fe(0)] and during microbial electrosynthesis have been considered support for a direct electron uptake in these microbial processes. However, the underlying molecular mechanisms of direct electron uptake are unknown. We investigated the electron uptake characteristics of the Fe(0)-corroding and electromethanogenic archaeonMethanococcus maripaludisand discovered that free, surface-associated redox enzymes, such as hydrogenases and presumably formate dehydrogenases, are sufficient to mediate an apparent direct electron uptake. In genetic and biochemical experiments, we showed that these enzymes, which are released from cells during routine culturing, catalyze the formation of H2or formate when sorbed to an appropriate redox-active surface. These low-molecular-weight products are rapidly consumed byM. maripaludiscells when present, thereby preventing their accumulation to any appreciable or even detectable level. Rates of H2and formate formation by cell-free spent culture medium were sufficient to explain the observed rates of methane formation from Fe(0) and cathode-derived electrons by wild-typeM. maripaludisas well as by a mutant strain carrying deletions in all catabolic hydrogenases. Our data collectively show that cell-derived free enzymes can mimic direct extracellular electron transfer during Fe(0) corrosion and microbial electrosynthesis and may represent an ecologically important but so far overlooked mechanism in biological electron transfer.IMPORTANCEThe intriguing trait of some microbial organisms to engage in direct electron transfer is thought to be widespread in nature. Consequently, direct uptake of electrons into microbial cells from solid surfaces is assumed to have a significant impact not only on fundamental microbial and biogeochemical processes but also on applied bioelectrochemical systems, such as microbial electrosynthesis and biocorrosion. This study provides a simple mechanistic explanation for frequently observed fast electron uptake kinetics in microbiological systems without a direct transfer: free, cell-derived enzymes can interact with cathodic surfaces and catalyze the formation of intermediates that are rapidly consumed by microbial cells. This electron transfer mechanism likely plays a significant role in various microbial electron transfer reactions in the environment.

scholarly journals Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “Candidatus Tenderia electrophaga”

mSystems ◽  
2017 ◽  
Vol 2 (2) ◽  
Author(s):  
Brian J. Eddie ◽  
Zheng Wang ◽  
W. Judson Hervey ◽  
Dagmar H. Leary ◽  
Anthony P. Malanoski ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Direct Electron Transfer ◽  
Electron Donors ◽  
Extracellular Electron Transfer ◽  
Uncultured Bacterium ◽  
Microbial Electrosynthesis ◽  
Electrode Cell ◽  
Electron Transfer Processes ◽  
New Evidence ◽  
Insight Into

ABSTRACT Bacteria that directly use electrodes as metabolic electron donors (biocathodes) have been proposed for applications ranging from microbial electrosynthesis to advanced bioelectronics for cellular communication with machines. However, just as we understand very little about oxidation of analogous natural insoluble electron donors, such as iron oxide, the organisms and extracellular electron transfer (EET) pathways underlying the electrode-cell direct electron transfer processes are almost completely unknown. Biocathodes are a stable biofilm cultivation platform to interrogate both the rate and mechanism of EET using electrochemistry and to study the electroautotrophic organisms that catalyze these reactions. Here we provide new evidence supporting the hypothesis that the uncultured bacterium “Candidatus Tenderia electrophaga” directly couples extracellular electron transfer to CO2 fixation. Our results provide insight into developing biocathode technology, such as microbial electrosynthesis, as well as advancing our understanding of chemolithoautotrophy. Biocathodes provide a stable electron source to drive reduction reactions in electrotrophic microbial electrochemical systems. Electroautotrophic biocathode communities may be more robust than monocultures in environmentally relevant settings, but some members are not easily cultivated outside the electrode environment. We previously used metagenomics and metaproteomics to propose a pathway for coupling extracellular electron transfer (EET) to carbon fixation in “Candidatus Tenderia electrophaga,” an uncultivated but dominant member of an electroautotrophic biocathode community. Here we validate and refine this proposed pathway using metatranscriptomics of replicate aerobic biocathodes poised at the growth potential level of 310 mV and the suboptimal 470 mV (versus the standard hydrogen electrode). At both potentials, transcripts were more abundant from “Ca. Tenderia electrophaga” than from any other constituent, and its relative activity was positively correlated with current. Several genes encoding key components of the proposed “Ca. Tenderia electrophaga” EET pathway were more highly expressed at 470 mV, consistent with a need for cells to acquire more electrons to obtain the same amount of energy as at 310 mV. These included cyc2, encoding a homolog of a protein known to be involved in iron oxidation. Mean expression of all CO2 fixation-related genes is 0.27 log2-fold higher at 310 mV, indicating that reduced energy availability at 470 mV decreased CO2 fixation. Our results substantiate the claim that “Ca. Tenderia electrophaga” is the key electroautotroph, which will help guide further development of this community for microbial electrosynthesis. IMPORTANCE Bacteria that directly use electrodes as metabolic electron donors (biocathodes) have been proposed for applications ranging from microbial electrosynthesis to advanced bioelectronics for cellular communication with machines. However, just as we understand very little about oxidation of analogous natural insoluble electron donors, such as iron oxide, the organisms and extracellular electron transfer (EET) pathways underlying the electrode-cell direct electron transfer processes are almost completely unknown. Biocathodes are a stable biofilm cultivation platform to interrogate both the rate and mechanism of EET using electrochemistry and to study the electroautotrophic organisms that catalyze these reactions. Here we provide new evidence supporting the hypothesis that the uncultured bacterium “Candidatus Tenderia electrophaga” directly couples extracellular electron transfer to CO2 fixation. Our results provide insight into developing biocathode technology, such as microbial electrosynthesis, as well as advancing our understanding of chemolithoautotrophy.

scholarly journals Metatranscriptomics supports mechanism for biocathode electroautotrophy by “Candidatus Tenderia electrophaga”

2016 ◽  
Author(s):  
Brian J. Eddie ◽  
Zheng Wang ◽  
W. Judson Hervey ◽  
Dagmar H. Leary ◽  
Anthony P. Malanoski ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Carbon Fixation ◽  
Direct Electron Transfer ◽  
Digital Pcr ◽  
Electron Donors ◽  
Growth Potential ◽  
Extracellular Electron Transfer ◽  
Hydrogen Electrode ◽  
Uncultured Bacterium ◽  
Microbial Electrosynthesis

AbstractBiocathodes provide a stable electron source to drive reduction reactions in electrotrophic microbial electrochemical systems. Electroautotrophic biocathode communities may be more robust than monocultures in environmentally relevant settings, but some members are not easily cultivated outside of the electrode environment. We previously used metagenomics and metaproteomics to propose a pathway for coupling extracellular electron transfer (EET) to carbon fixation in “Candidatus Tenderia electrophaga”, an uncultivated but dominant member of the Biocathode-MCL electroautotrophic community. Here we validate and refine this proposed pathway using differential metatranscriptomics of replicate MCL reactors poised at the growth potential 310 mV and the suboptimal 470 mV (vs. standard hydrogen electrode). At both potentials, transcripts from “Ca. Tenderia electrophaga” were more abundant than from any other organism and its relative activity was positively correlated with current. Several genes encoding key components of the proposed “Ca. Tenderia electrophaga” EET pathway were more highly expressed at 470 mV, consistent with a need for cells to acquire more electrons to obtain the same amount of energy as at 310 mV. These included cyc2, encoding a homolog of a protein known to be involved in iron oxidation, confirmed to be differentially expressed by droplet digital PCR of independent biological replicates. Average expression of all CO2 fixation related genes is 1.23-fold higher at 310 mV, indicating that reduced energy availability at 470 mV decreased CO2 fixation. Our results substantiate the claim that “Ca. Tenderia electrophaga” is the key MCL electroautotroph, which will help guide further development of this community for microbial electrosynthesis.IMPORTANCEBacteria that directly use electrodes as metabolic electron donors (biocathodes) have been proposed for applications ranging from microbial electrosynthesis to advanced bioelectronics for cellular communication with machines. However, just as we understand very little about oxidation of analogous natural insoluble electron donors, such as iron oxide, the organisms and extracellular electron transfer (EET) pathways underlying the electrode-cell direct electron transfer processes are almost completely unknown. Biocathodes are a stable biofilm cultivation platform to interrogate both the rate and mechanism of EET using electrochemistry and study the electroautotrophic organisms that catalyze these reactions. Here we provide new evidence supporting the hypothesis that the uncultured bacterium “Candidatus Tenderia electrophaga” directly couples extracellular electron transfer to CO2 fixation. Our results provide insight into developing biocathode technology, such as microbial electrosynthesis, as well as advancing our understanding of chemolithoautotrophy.

Respiratory Au nucleation and microelectrode techniques reveal key features of bacterial conductive matrix

2020 ◽  
Vol 7 (10) ◽  
pp. 3189-3200
Author(s):  
María Victoria Ordóñez ◽  
Luciana Robuschi ◽  
Cristina Elena Hoppe ◽  
Juan Pablo Busalmen
Keyword(s):  
Gold Nanoparticles ◽  
Electron Transfer ◽  
Transfer Mechanism ◽  
Extracellular Electron Transfer ◽  
Electron Transfer Mechanism ◽  
Key Features ◽  
Microelectrode Techniques

Key elements of Geobacter's extracellular electron transfer mechanism are characterized combining respiratory formed gold nanoparticles with spectro-electrochemical and microelectrode techniques.

Extracellular electron transfer through microbial reduction of solid-phase humic substances

2010 ◽  
Vol 3 (6) ◽  
pp. 417-421 ◽  
Author(s):  
Eric E. Roden ◽  
Andreas Kappler ◽  
Iris Bauer ◽  
Jie Jiang ◽  
Andrea Paul ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Humic Substances ◽  
Solid Phase ◽  
Microbial Reduction ◽  
Extracellular Electron Transfer

scholarly journals A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria

Nature ◽  
2018 ◽  
Vol 562 (7725) ◽  
pp. 140-144 ◽  
Author(s):  
Samuel H. Light ◽  
Lin Su ◽  
Rafael Rivera-Lugo ◽  
Jose A. Cornejo ◽  
Alexander Louie ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Transfer Mechanism ◽  
Extracellular Electron Transfer ◽  
Gram Positive ◽  
Electron Transfer Mechanism ◽  
Gram Positive Bacteria

scholarly journals Methane-Linked Mechanisms of Electron Uptake from Cathodes byMethanosarcina barkeri

mBio ◽  
2019 ◽  
Vol 10 (2) ◽  
Author(s):  
Annette R. Rowe ◽  
Shuai Xu ◽  
Emily Gardel ◽  
Arpita Bose ◽  
Peter Girguis ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Methane Production ◽  
Extracellular Enzymes ◽  
Solid Phase ◽  
Electrochemical Techniques ◽  
Methanosarcina Barkeri ◽  
Extracellular Electron Transfer ◽  
Hydrogen Electrode ◽  
Content Type ◽  
Wide Range

ABSTRACTTheMethanosarcinales, a lineage of cytochrome-containing methanogens, have recently been proposed to participate in direct extracellular electron transfer interactions within syntrophic communities. To shed light on this phenomenon, we applied electrochemical techniques to measure electron uptake from cathodes byMethanosarcina barkeri, which is an important model organism that is genetically tractable and utilizes a wide range of substrates for methanogenesis. Here, we confirm the ability ofM. barkerito perform electron uptake from cathodes and show that this cathodic current is linked to quantitative increases in methane production. The underlying mechanisms we identified include, but are not limited to, a recently proposed association between cathodes and methanogen-derived extracellular enzymes (e.g., hydrogenases) that can facilitate current generation through the formation of reduced and diffusible methanogenic substrates (e.g., hydrogen). However, after minimizing the contributions of such extracellular enzymes and using a mutant lacking hydrogenases, we observe a lower-potential hydrogen-independent pathway that facilitates cathodic activity coupled to methane production inM. barkeri. Our electrochemical measurements of wild-type and mutant strains point to a novel and hydrogenase-free mode of electron uptake with a potential near −484 mV versus standard hydrogen electrode (SHE) (over 100 mV more reduced than the observed hydrogenase midpoint potential under these conditions). These results suggest thatM. barkerican perform multiple modes (hydrogenase-mediated and free extracellular enzyme-independent modes) of electrode interactions on cathodes, including a mechanism pointing to a direct interaction, which has significant applied and ecological implications.IMPORTANCEMethanogenic archaea are of fundamental applied and environmental relevance. This is largely due to their activities in a wide range of anaerobic environments, generating gaseous reduced carbon that can be utilized as a fuel source. While the bioenergetics of a wide variety of methanogens have been well studied with respect to soluble substrates, a mechanistic understanding of their interaction with solid-phase redox-active compounds is limited. This work provides insight into solid-phase redox interactions inMethanosarcinaspp. using electrochemical methods. We highlight a previously undescribed mode of electron uptake from cathodes that is potentially informative of direct interspecies electron transfer interactions in theMethanosarcinales.

scholarly journals In-Situ Sensing of Microbial Growth Phases via Two-Terminal Cyclic Voltammetry

2020 ◽  
Author(s):  
Arindam Kushagra ◽  
Diyasa Bazal ◽  
Anup Kumar Pradhan ◽  
Pratyusha Ghosh ◽  
Akshaya Pandey
Keyword(s):  
Electron Transfer ◽  
Cyclic Voltammetry ◽  
Microbial Growth ◽  
Extracellular Polymeric Substances ◽  
Electrochemical Sensors ◽  
Extracellular Electron Transfer ◽  
Growth Phases ◽  
Electron Transfer Mechanism ◽  
Temporal Area ◽  
In Situ Sensing

Microbial growth has been of prime importance to the researchers in health and biotechnology industries. It has been known to be closely associated to the secretion of extracellular polymeric substances that help in the formation of colonies. Inter-microbial communication happens within such colonies by means of extracellular electron transfer mediated by the aforementioned polymeric substances. Conventionally, different phases of microbial growth are monitored with the aid of a traditional UV-Visible spectrophotometer by measuring the optical density of the liquid medium at 280 nm. In this paper, we have developed an alternative novel way to sense different growth phases employing electrochemical means i.e. two-terminal cyclic voltammetry. This cyclic voltammetry relies on the extracellular electron transfer mechanism taking place via the polymeric substances secreted by the microorganisms, measured by the temporal area changes in the current-voltage hysteresis curves in the inoculated nutrient broth. This work paves a new way to detect the biological activity in the medium, which can be directly correlated to the population of microorganisms. It would be of immense interest to scientists and researchers working in the field of microbiology as well as in development of biosensors, electrochemical sensors etc. which would be helpful in absence of traditional spectrophotometers.

scholarly journals Combined electrochemical and microscopic study of porous enzymatic electrodes with direct electron transfer mechanism

RSC Advances ◽  
2014 ◽  
Vol 4 (69) ◽  
pp. 36471-36479 ◽  
Author(s):  
M. Varničić ◽  
K. Bettenbrock ◽  
D. Hermsdorf ◽  
T. Vidaković-Koch ◽  
K. Sundmacher
Keyword(s):  
Electron Transfer ◽  
Microscopic Study ◽  
Direct Electron Transfer ◽  
Transfer Mechanism ◽  
Complex Relationship ◽  
Electron Transfer Mechanism ◽  
Preparation Route ◽  
Structure And Activity ◽  
Insight Into

In the present work electrochemical and microscopic methods have been utilized to get more insight into the complex relationship between the preparation route, structure and activity of porous enzymatic electrodes.

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