Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis

ABSTRACT 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 i...

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Autores principales:	Jörg S. Deutzmann, Merve Sahin, Alfred M. Spormann
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ee172cd14e9b4f8d82752d1b9e6505ad
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spelling	oai:doaj.org-article:ee172cd14e9b4f8d82752d1b9e6505ad2021-11-15T15:41:33ZExtracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis10.1128/mBio.00496-152150-7511https://doaj.org/article/ee172cd14e9b4f8d82752d1b9e6505ad2015-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00496-15https://doaj.org/toc/2150-7511ABSTRACT 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.Jörg S. DeutzmannMerve SahinAlfred M. SpormannAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 2 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Jörg S. Deutzmann Merve Sahin Alfred M. Spormann Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis
description	ABSTRACT 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.
format	article
author	Jörg S. Deutzmann Merve Sahin Alfred M. Spormann
author_facet	Jörg S. Deutzmann Merve Sahin Alfred M. Spormann
author_sort	Jörg S. Deutzmann
title	Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis
title_short	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_sort	extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/ee172cd14e9b4f8d82752d1b9e6505ad
work_keys_str_mv	AT jorgsdeutzmann extracellularenzymesfacilitateelectronuptakeinbiocorrosionandbioelectrosynthesis AT mervesahin extracellularenzymesfacilitateelectronuptakeinbiocorrosionandbioelectrosynthesis AT alfredmspormann extracellularenzymesfacilitateelectronuptakeinbiocorrosionandbioelectrosynthesis
_version_	1718427679849447424

Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis

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