Spatially Resolved Electron Transport through Anode‐Respiring <i>Geobacter sulfurreducens</i> Biofilms: Controls and Constraints

He, Xiaojia; Chadwick, Grayson L.; Otero, Fernanda Jiménez; Orphan, Victoria J.; Meile, Christof

doi:10.1002/celc.202100111

Cited by 9 publications

(8 citation statements)

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“…Our results showing higher current densities in extABCD + biofilms as a result of more densely packed cells and higher 15 N incorporation rates within a similar 0- to 10-μm active zone shows that this steep stratification favoring the region near the electrode also occurs in extABCD + biofilms. However, our results show evidence for a new penalty at the electrode-biofilm interface in extABCD + biofilms compared to wild-type biofilms, consistent with previously modeled effects of proton accumulation due to the increased anabolic rate beginning to limit current production ( 26 , 27 ).…”

Section: Discussionsupporting

confidence: 91%

“…A second form of growth rate decline was also observed within the 2 μm closest to the electrode, suggesting acidification nearest to the electrode caused by the higher metabolic rates of extABCD + . The difference between peak 15 N fractional abundance and levels near the electrode in wild-type samples was 0.15% but increased to 0.38% for the extABCD + strain, suggesting that buffering diffusion limitations previously predicted through modeling ( 26 , 27 ) might play a more significant role as the anabolic rate increases.…”

Section: Resultsmentioning

confidence: 78%

“…When biofilms use electrodes as electron acceptors, the metabolic state of cells is heterogeneous, or metabolically stratified, due to cells closest to the electrode experiencing the highest redox potential and overactive cells possibly poisoning themselves due to acidification ( 25 , 26 ). In all electrode-based observations, isotope incorporation of labeled carbon and nitrogen within current-producing biofilms is highest within the first 10 μm ( 25 ) and the redox state of cytochromes is most oxidized at the electrode-biofilm interface, suggesting that the environment closest to the electrode remains favorable even when buried beneath tens of micrometers of biomass ( 36 – 40 ).…”

Section: Discussionmentioning

confidence: 99%

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Evidence of a Streamlined Extracellular Electron Transfer Pathway from Biofilm Structure, Metabolic Stratification, and Long-Range Electron Transfer Parameters

Otero

Chadwick

Yates

et al. 2021

Appl Environ Microbiol

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A strain of Geobacter sulfurreducens , an organism capable of respiring solid extracellular substrates, lacking four out of five outer membrane cytochrome complexes (strain extABCD + ) grows faster and produces greater current density compared to wild type grown under identical conditions. To understand cellular and biofilm modifications altered in extABCD + responsible for this increased performance, biofilms grown using electrodes as terminal electron acceptors were sectioned and imaged using electron microscopy to determine changes in thickness and cell density, while parallel biofilms incubated in the presence of nitrogen and carbon isotopes were analyzed using NanoSIMS to quantify and localize anabolic activity. Long-distance electron transfer parameters were measured for wild type and extABCD + biofilms spanning 5 μm gaps. Our results reveal that extABCD + biofilms achieved higher current densities through the additive effects of denser cell packing close to the electrode (based on electron microscopy), combined with higher metabolic rates per cell compared to wild type (based on increased rates of 15 N incorporation). We also observed an increased rate of electron transfer through extABCD + vs. wild-type biofilms, suggesting that denser biofilms resulting from the deletion of unnecessary multi-heme cytochromes streamlines electron transfer to electrodes. The combination of imaging, physiological and electrochemical data confirms that engineered electrogenic bacteria are capable of producing more current per cell and, in combination with higher biofilm density and electron diffusion rates, can produce a higher final current density than wild type. Importance Current-producing biofilms in microbial electrochemical systems could potentially sustain technologies ranging from wastewater treatment to bioproduction of electricity if the maximum current produced could be increased and current production start-up times after inoculation could be reduced. Enhancing the current output of microbial electrochemical systems has been mostly approached by engineering physical components of reactors and electrodes. Here, we show that biofilms formed by a Geobacter sulfurreducens strain producing ∼1.4x higher current compared to wild type results from a combination of denser cell packing and higher anabolic activity, enabled by an increased rate of electron diffusion through the biofilms. Our results confirm that it is possible to engineer electrode-specific G. sulfurreducens strains with both faster growth on electrodes and streamlined electron transfer pathways for enhanced current production.

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Section: Discussionsupporting

confidence: 91%

Section: Resultsmentioning

confidence: 78%

Section: Discussionmentioning

confidence: 99%

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Evidence of a Streamlined Extracellular Electron Transfer Pathway from Biofilm Structure, Metabolic Stratification, and Long-Range Electron Transfer Parameters

Otero

Chadwick

Yates

et al. 2021

Appl Environ Microbiol

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“…Having multiple options for linking electron flow to proton extrusion may allow Geobacter to dominate in energy-limited aquifers selecting for low growth yield and persistence, while still retaining an ability to switch to a high cellular yield during a sudden influx of electron donors, similar to what occurs during environmental biostimulation. In the laboratory, this could also explain how Geobacter is commonly obtained in both enrichments selecting for rapid growth, and on electrodes that create persistent redox-stratified biofilms (Chadwick et al, 2019;He et al, 2021;Snider et al, 2012).…”

Section: Our Data Showing Activation By Low Potential Help Explainmentioning

confidence: 99%

Geobacter sulfurreducens inner membrane cytochrome CbcBA controls electron transfer and growth yield near the energetic limit of respiration

Joshi

Chan

Bond

2021

Molecular Microbiology

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Life generates cellular energy by linking electron donor oxidation to acceptor reduction. Each electron source and sink has an inherent potential which together defines the maximum amount of energy available when electrons are exchanged in coupled reactions. For example, the difference in NO − 3 and Fe(III)(oxyhydr)oxides reduction potentials is more than half a volt, representing an additional 60 kJ/mol e − available during nitrate reduction when acetate is the donor (E°′ of NO − 3 ∕NO − 2 = +0.43 V vs. E°′ of Fe(III) (oxyhydr)oxides/ Fe(II) ~−0.2 V vs. standard hydrogen electrode [SHE]) (Fischer, 1987;

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“…Recently, a finite distance over which extracellular electron transport sustains metabolic activity was documented in biofilms of Geobacter sulfurreducens (24). These results suggest that the extent to which conductive biomolecules can support optimal cell growth away from an electrode surface is limited (24,25). Using a similar experimental approach, a drop in activity with distance between electron donors (archaea) and acceptors (bacteria) was not observed in AOM aggregates (17)(18)(19).…”

mentioning

confidence: 88%

Controls on Interspecies Electron Transport and Size Limitation of Anaerobically Methane-Oxidizing Microbial Consortia

Chadwick

Kempes

et al. 2021

mBio

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About 382 Tg yr−1 of methane rising through the seafloor is oxidized anaerobically (W. S. Reeburgh, Chem Rev 107:486–513, 2007, https://doi.org/10.1021/cr050362v), preventing it from reaching the atmosphere, where it acts as a strong greenhouse gas. Microbial consortia composed of anaerobic methanotrophic archaea and sulfate-reducing bacteria couple the oxidation of methane to the reduction of sulfate under anaerobic conditions via a syntrophic process. Recent experimental studies and modeling efforts indicate that direct interspecies electron transfer (DIET) is involved in this syntrophy. Here, we explore a fluorescent in situ hybridization-nanoscale secondary ion mass spectrometry data set of large, segregated anaerobic oxidation of methane (AOM) consortia that reveal a decline in metabolic activity away from the archaeal-bacterial interface and use a process-based model to identify the physiological controls on rates of AOM. Simulations reproducing the observational data reveal that ohmic resistance and activation loss are the two main factors causing the declining metabolic activity, where activation loss dominated at a distance of <8 μm. These voltage losses limit the maximum spatial distance between syntrophic partners with model simulations, indicating that sulfate-reducing bacterial cells can remain metabolically active up to ∼30 μm away from the archaeal-bacterial interface. Model simulations further predict that a hybrid metabolism that combines DIET with a small contribution of diffusive exchange of electron donors can offer energetic advantages for syntrophic consortia. IMPORTANCE Anaerobic oxidation of methane is a globally important, microbially mediated process reducing the emission of methane, a potent greenhouse gas. In this study, we investigate the mechanism of how a microbial consortium consisting of archaea and bacteria carries out this process and how these organisms interact with each other through the sharing of electrons. We present a process-based model validated by novel experimental measurements of the metabolic activity of individual, phylogenetically identified cells in very large (>20-μm-diameter) microbial aggregates. Model simulations indicate that extracellular electron transfer between archaeal and bacterial cells within a consortium is limited by potential losses and suggest that a flexible use of electron donors can provide energetic advantages for syntrophic consortia.

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

Abstract: Supporting information for this article is given via a link at the end of the document.

Cited by 9 publications

References 124 publications

Evidence of a Streamlined Extracellular Electron Transfer Pathway from Biofilm Structure, Metabolic Stratification, and Long-Range Electron Transfer Parameters

Evidence of a Streamlined Extracellular Electron Transfer Pathway from Biofilm Structure, Metabolic Stratification, and Long-Range Electron Transfer Parameters

Geobacter sulfurreducens inner membrane cytochrome CbcBA controls electron transfer and growth yield near the energetic limit of respiration

Controls on Interspecies Electron Transport and Size Limitation of Anaerobically Methane-Oxidizing Microbial Consortia

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