Extracellular enzymes facilitate Electron uptake in biocorrosion and Bioelectrosynthesis
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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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Studies of microbes that grow on native iron and on electrodes suggest that side activities of extracellular enzymes might be able to substitute for hydrogenases.
“Studies of microbes that grow on native iron and on electrodes suggest that side activities of extracellular enzymes might be able to substitute for hydrogenases (Deutzmann et al., 2015).”
From Serpentinization as the source of energy, electrons, organics, catalysts, nutrients and pH gradients for the origin of LUCA and life (2023) · cites this paper as Deutzmann et al., 2015
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- 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.
- Venue
- mBio
- Publisher
- American Society for Microbiology
- Published
- 2015-05
- Volume
- 6
- Issue
- 2
- ISSN
- 2150-7511 (ISSN-L)
- 2161-2129
- 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
- gold
- doi.org
- 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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