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Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis

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...

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Autores principales: Deutzmann, Jörg S., Sahin, Merve, Spormann, Alfred M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society of Microbiology 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4453541/
https://www.ncbi.nlm.nih.gov/pubmed/25900658
http://dx.doi.org/10.1128/mBio.00496-15
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author Deutzmann, Jörg S.
Sahin, Merve
Spormann, Alfred M.
author_facet Deutzmann, Jörg S.
Sahin, Merve
Spormann, Alfred M.
author_sort Deutzmann, Jörg S.
collection PubMed
description 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 H(2) 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 H(2) 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.
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spelling pubmed-44535412015-06-03 Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis Deutzmann, Jörg S. Sahin, Merve Spormann, Alfred M. mBio Research Article 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 H(2) 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 H(2) 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. American Society of Microbiology 2015-04-21 /pmc/articles/PMC4453541/ /pubmed/25900658 http://dx.doi.org/10.1128/mBio.00496-15 Text en Copyright © 2015 Deutzmann et al. http://creativecommons.org/licenses/by-nc-sa/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license (http://creativecommons.org/licenses/by-nc-sa/3.0/) , which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Deutzmann, Jörg S.
Sahin, Merve
Spormann, Alfred M.
Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis
title Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis
title_full Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis
title_fullStr Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis
title_full_unstemmed Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis
title_short Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis
title_sort extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4453541/
https://www.ncbi.nlm.nih.gov/pubmed/25900658
http://dx.doi.org/10.1128/mBio.00496-15
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