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Cited by 380Microbial Fuel Cells and BioremediationCorrosion Behavior and InhibitionMicrobial metabolism and enzyme function

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Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis

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Deutzmann, Jörg S., Sahin, Merve, Spormann, Alfred M.·2015·mBio
DOI 10.1128/mbio.00496-15PMC PMC4453541
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Abstract

UNLABELLED: Direct, 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 archaeon Methanococcus maripaludis and 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 H2 or formate when sorbed to an appropriate redox-active surface. These low-molecular-weight products are rapidly consumed by M. maripaludis cells when present, thereby preventing their accumulation to any appreciable or even detectable level. Rates of H2 and 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-type M. maripaludis as 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. IMPORTANCE: The 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.

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Figures

FIG 1 Methane, hydrogen, and formate formation during Fe(0) corrosion by M. maripaludis wild type (MM901) cells, hydrogenase deletion mutant (MM1284) cells, and respective spent cell-free culture medium with Fe(0) granules [0.4 g Fe(0) and 15 ml medium in 60-ml serum vials]. (a) Methane formation by MM901 cells (inset, MM1284 cells); no methane was formed in SCM-amended vials or medium controls; (b) formate formation by SCM of strains MM901 and MM1284; formate was barely detectable with living cells or in medium controls; (c) hydrogen formation by spent culture medium of strain MM901. Triangles, MM901; diamonds, MM1284; circles, medium control; open symbols, SCM; filled symbols, living cells.
FIG 1 Methane, hydrogen, and formate formation during Fe(0) corrosion by M. maripaludis wild type (MM901) cells, hydrogenase deletion mutant (MM1284) cells, and respective spent cell-free culture medium with Fe(0) granules [0.4 g Fe(0) and 15 ml medium in 60-ml serum vials]. (a) Methane formation by MM901 cells (inset, MM1284 cells); no methane was formed in SCM-amended vials or medium controls; (b) formate formation by SCM of strains MM901 and MM1284; formate was barely detectable with living cells or in medium controls; (c) hydrogen formation by spent culture medium of strain MM901. Triangles, MM901; diamonds, MM1284; circles, medium control; open symbols, SCM; filled symbols, living cells.CC BY-NC-SA · PubMed Central
FIG 2 Hydrogen and formate formation by spent cell-free culture medium of M. maripaludis wild-type (MM901) and hydrogenase deletion mutant (MM1284) strains on graphite cathodes. (a) Formate formation on graphite cathodes; (b) hydrogen formation on graphite cathodes. Triangles, MM901; diamonds, MM1284; circles, medium control. Electrode potentials as indicated. (c) Surface attachment and long-term stability of the catalytic activity of MM901 SCM at a cathode potential of −600 mV. Above-background current consumption was observed for several weeks in a bioelectrochemical reactor amended with cell-free spent medium of strain MM901. Current consumption increased after the entire medium was exchanged in the cathode chamber (indicated by arrows). This current increase was likely due to replenished substrate supply (CO2 and H+) and indicates surface attachment of the catalytic activity. Background current consumption without SCM is indicated by a gray line.
FIG 2 Hydrogen and formate formation by spent cell-free culture medium of M. maripaludis wild-type (MM901) and hydrogenase deletion mutant (MM1284) strains on graphite cathodes. (a) Formate formation on graphite cathodes; (b) hydrogen formation on graphite cathodes. Triangles, MM901; diamonds, MM1284; circles, medium control. Electrode potentials as indicated. (c) Surface attachment and long-term stability of the catalytic activity of MM901 SCM at a cathode potential of −600 mV. Above-background current consumption was observed for several weeks in a bioelectrochemical reactor amended with cell-free spent medium of strain MM901. Current consumption increased after the entire medium was exchanged in the cathode chamber (indicated by arrows). This current increase was likely due to replenished substrate supply (CO2 and H+) and indicates surface attachment of the catalytic activity. Background current consumption without SCM is indicated by a gray line.CC BY-NC-SA · PubMed Central
FIG 3 Reversibility of spent cell-free culture medium-mediated hydrogen and formate formation in bioelectrochemical reactors at −200 mV. Low background current consumption is observed in an N2-CO2 (80/20) atmosphere in SCM-amended (solid black line) and uninoculated medium (gray line) (1). Upon addition of 10% H2, current is generated only in the presence of SCM (2), current returns to background after replacing the gas phase with N2-CO2 (3), current is generated upon addition of 100 mM formate only in the presence of SCM (4), and replacing the gas phase by H2-CO2 (80/20) further increases current generation by SCM (5). Current spikes between treatments are due to disconnection of the electrochemical reactors from the potentiostat during handling.
FIG 3 Reversibility of spent cell-free culture medium-mediated hydrogen and formate formation in bioelectrochemical reactors at −200 mV. Low background current consumption is observed in an N2-CO2 (80/20) atmosphere in SCM-amended (solid black line) and uninoculated medium (gray line) (1). Upon addition of 10% H2, current is generated only in the presence of SCM (2), current returns to background after replacing the gas phase with N2-CO2 (3), current is generated upon addition of 100 mM formate only in the presence of SCM (4), and replacing the gas phase by H2-CO2 (80/20) further increases current generation by SCM (5). Current spikes between treatments are due to disconnection of the electrochemical reactors from the potentiostat during handling.CC BY-NC-SA · PubMed Central
FIG 4 Acetate and hydrogen formation by S. sphaeroides cells and cell-free spent culture medium on graphite cathodes poised at −500 mV. (a) Only intact cells of S. sphaeroides (filled triangles) form acetate. (b) Cell-free spent culture medium (SCM; open triangles) and intact cells (filled triangles) form H2 initially, but H2 accumulates to higher concentrations only without intact cells. Open circles, medium control; stars, heat-inactivated SCM controls.
FIG 4 Acetate and hydrogen formation by S. sphaeroides cells and cell-free spent culture medium on graphite cathodes poised at −500 mV. (a) Only intact cells of S. sphaeroides (filled triangles) form acetate. (b) Cell-free spent culture medium (SCM; open triangles) and intact cells (filled triangles) form H2 initially, but H2 accumulates to higher concentrations only without intact cells. Open circles, medium control; stars, heat-inactivated SCM controls.CC BY-NC-SA · PubMed Central

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Research works printed but not linked: 1

  1. Tate R, III. 2002. Microbiology and enzymology of carbon and nitrogen cycling, p 227–248. In Burns RG, Dick RP (ed), Enzymes in the environment. Marcel Dekker, New York, NY.

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Metadata

Authors
Deutzmann, J. S., Sahin, M., & Spormann, A. M.
Affiliations
  • Stanford University (US)
  • Department of Civil and Environmental Engineering, Stanford University, Stanford, California, USA
Corresponding author
Spormann, Alfred M.
ORCID
Venue
mBio
Publisher
American Society for Microbiology
Published
2015-05
Volume
6
Issue
2
ISSN
  • 2150-7511 (ISSN-L)
  • 2161-2129
DOI
10.1128/mbio.00496-15
PMC
PMC4453541
OpenAlex
W2141860790
Cited by
379
References
66
Citations by year
2026: 18 · 2025: 21 · 2024: 29 · 2023: 31 · 2022: 39 · 2021: 29 · 2020: 47 · 2019: 43 · 2018: 41 · 2017: 40 · 2016: 31 · 2015: 10
FWCI
29.27
Type
journal article
Language
en
Open access
Licence
Locations
  • mBio (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
  • Physical Sciences › Materials Science › Materials Chemistry › Corrosion Behavior and Inhibition
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
Keywords
extracellular enzymes, direct electron transfer, microbiologically influenced corrosion, microbial electrosynthesis, Methanococcus maripaludis, iron corrosion, hydrogenase, formate dehydrogenase, hydrogen production, methane production, bioelectrochemical systems
MeSH terms
Corrosion, Electron Transport, Formates, Hydrogen, Iron, Methane, Oxidoreductases, Methanococcus

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