Iron Corrosion via Direct Metal-Microbe Electron Transfer

ABSTRACT The concept that anaerobic microorganisms can directly accept electrons from Fe(0) has been controversial because direct metal-microbe electron transfer has previously only been indirectly inferred. Fe(0) oxidation was studied with Geobacter sulfurreducens strain ACL, an autotrophic strain...

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Autores principales:	Hai-Yan Tang, Dawn E. Holmes, Toshiyuki Ueki, Paola A. Palacios, Derek R. Lovley
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Geobacter autotroph cytochrome electromicrobiology extracellular electron transfer zero-valent iron Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0ff34ee07a8d4e8ba3cbc1bd80903202
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spelling	oai:doaj.org-article:0ff34ee07a8d4e8ba3cbc1bd809032022021-11-15T15:55:25ZIron Corrosion via Direct Metal-Microbe Electron Transfer10.1128/mBio.00303-192150-7511https://doaj.org/article/0ff34ee07a8d4e8ba3cbc1bd809032022019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00303-19https://doaj.org/toc/2150-7511ABSTRACT The concept that anaerobic microorganisms can directly accept electrons from Fe(0) has been controversial because direct metal-microbe electron transfer has previously only been indirectly inferred. Fe(0) oxidation was studied with Geobacter sulfurreducens strain ACL, an autotrophic strain that was previously shown to grow with electrons derived from a graphite cathode as the sole electron donor. Strain ACL grew with Fe(0) as the sole electron donor and fumarate as the electron acceptor. However, it appeared that at least a portion of the electron transfer was via H2 produced nonenzymatically from the oxidation of Fe(0) to Fe(II). H2, which accumulated in abiotic controls, was consumed during the growth of strain ACL, the cells were predominately planktonic, and genes for the uptake hydrogenase were highly expressed. Strain ACLHF was constructed to prevent growth on H2 or formate by deleting the genes for the uptake of hydrogenase and formate dehydrogenases from strain ACL. Strain ACLHF also grew with Fe(0) as the sole electron donor, but H2 accumulated in the culture, and cells heavily colonized Fe(0) surfaces with no visible planktonic growth. Transcriptomics suggested that the outer surface c-type cytochromes OmcS and OmcZ were important during growth of strain ACLHF on Fe(0). Strain ACLHF did not grow on Fe(0) if the gene for either of these cytochromes was deleted. The specific attachment of strain ACLHF to Fe(0), coupled with requirements for known extracellular electrical contacts, suggest that direct metal-microbe electron transfer is the most likely option for Fe(0) serving as an electron donor. IMPORTANCE The anaerobic corrosion of iron structures is expensive to repair and can be a safety and environmental concern. It has been known for over 100 years that the presence of anaerobic respiratory microorganisms can accelerate iron corrosion. Multiple studies have suggested that there are sulfate reducers, methanogens, and acetogens that can directly accept electrons from Fe(0) to support sulfate or carbon dioxide reduction. However, all of the strains studied can also use H2 as an electron donor for growth, which is known to be abiotically produced from Fe(0). Furthermore, no proteins definitely shown to function as extracellular electrical contacts with Fe(0) were identified. The studies described here demonstrate that direct electron transfer from Fe(0) can support anaerobic respiration. They also map out a simple genetic approach to the study of iron corrosion mechanisms in other microorganisms. A better understanding of how microorganisms promote iron corrosion is expected to lead to the development of strategies that can help reduce adverse impacts from this process.Hai-Yan TangDawn E. HolmesToshiyuki UekiPaola A. PalaciosDerek R. LovleyAmerican Society for MicrobiologyarticleGeobacterautotrophcytochromeelectromicrobiologyextracellular electron transferzero-valent ironMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Geobacter autotroph cytochrome electromicrobiology extracellular electron transfer zero-valent iron Microbiology QR1-502
spellingShingle	Geobacter autotroph cytochrome electromicrobiology extracellular electron transfer zero-valent iron Microbiology QR1-502 Hai-Yan Tang Dawn E. Holmes Toshiyuki Ueki Paola A. Palacios Derek R. Lovley Iron Corrosion via Direct Metal-Microbe Electron Transfer
description	ABSTRACT The concept that anaerobic microorganisms can directly accept electrons from Fe(0) has been controversial because direct metal-microbe electron transfer has previously only been indirectly inferred. Fe(0) oxidation was studied with Geobacter sulfurreducens strain ACL, an autotrophic strain that was previously shown to grow with electrons derived from a graphite cathode as the sole electron donor. Strain ACL grew with Fe(0) as the sole electron donor and fumarate as the electron acceptor. However, it appeared that at least a portion of the electron transfer was via H2 produced nonenzymatically from the oxidation of Fe(0) to Fe(II). H2, which accumulated in abiotic controls, was consumed during the growth of strain ACL, the cells were predominately planktonic, and genes for the uptake hydrogenase were highly expressed. Strain ACLHF was constructed to prevent growth on H2 or formate by deleting the genes for the uptake of hydrogenase and formate dehydrogenases from strain ACL. Strain ACLHF also grew with Fe(0) as the sole electron donor, but H2 accumulated in the culture, and cells heavily colonized Fe(0) surfaces with no visible planktonic growth. Transcriptomics suggested that the outer surface c-type cytochromes OmcS and OmcZ were important during growth of strain ACLHF on Fe(0). Strain ACLHF did not grow on Fe(0) if the gene for either of these cytochromes was deleted. The specific attachment of strain ACLHF to Fe(0), coupled with requirements for known extracellular electrical contacts, suggest that direct metal-microbe electron transfer is the most likely option for Fe(0) serving as an electron donor. IMPORTANCE The anaerobic corrosion of iron structures is expensive to repair and can be a safety and environmental concern. It has been known for over 100 years that the presence of anaerobic respiratory microorganisms can accelerate iron corrosion. Multiple studies have suggested that there are sulfate reducers, methanogens, and acetogens that can directly accept electrons from Fe(0) to support sulfate or carbon dioxide reduction. However, all of the strains studied can also use H2 as an electron donor for growth, which is known to be abiotically produced from Fe(0). Furthermore, no proteins definitely shown to function as extracellular electrical contacts with Fe(0) were identified. The studies described here demonstrate that direct electron transfer from Fe(0) can support anaerobic respiration. They also map out a simple genetic approach to the study of iron corrosion mechanisms in other microorganisms. A better understanding of how microorganisms promote iron corrosion is expected to lead to the development of strategies that can help reduce adverse impacts from this process.
format	article
author	Hai-Yan Tang Dawn E. Holmes Toshiyuki Ueki Paola A. Palacios Derek R. Lovley
author_facet	Hai-Yan Tang Dawn E. Holmes Toshiyuki Ueki Paola A. Palacios Derek R. Lovley
author_sort	Hai-Yan Tang
title	Iron Corrosion via Direct Metal-Microbe Electron Transfer
title_short	Iron Corrosion via Direct Metal-Microbe Electron Transfer
title_full	Iron Corrosion via Direct Metal-Microbe Electron Transfer
title_fullStr	Iron Corrosion via Direct Metal-Microbe Electron Transfer
title_full_unstemmed	Iron Corrosion via Direct Metal-Microbe Electron Transfer
title_sort	iron corrosion via direct metal-microbe electron transfer
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/0ff34ee07a8d4e8ba3cbc1bd80903202
work_keys_str_mv	AT haiyantang ironcorrosionviadirectmetalmicrobeelectrontransfer AT dawneholmes ironcorrosionviadirectmetalmicrobeelectrontransfer AT toshiyukiueki ironcorrosionviadirectmetalmicrobeelectrontransfer AT paolaapalacios ironcorrosionviadirectmetalmicrobeelectrontransfer AT derekrlovley ironcorrosionviadirectmetalmicrobeelectrontransfer
_version_	1718427134796496896

Iron Corrosion via Direct Metal-Microbe Electron Transfer

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