CO2/HCO3− Accelerates Iron Reduction through Phenolic Compounds

In an oxygenic environment, poorly soluble Fe3+ must be reduced to meet the cellular Fe2+ demand. This study demonstrates that elevated CO2/HCO3− levels accelerate chemical Fe3+ reduction through phenolic compounds, thus increasing intracellular Fe2+ availability. A number of biological environments...

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Main Authors: Felix Müller, Johanna Rapp, Anna-Lena Hacker, André Feith, Ralf Takors, Bastian Blombach
Format: Article
Language:English
Published: American Society for Microbiology 2020-03-01
Series:mBio
Subjects:
Online Access:https://doi.org/10.1128/mBio.00085-20
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spelling doaj-75a7bb7fe4bc483cb236024e963c92db2021-07-02T08:40:16ZengAmerican Society for MicrobiologymBio2150-75112020-03-01112e00085-2010.1128/mBio.00085-20CO2/HCO3− Accelerates Iron Reduction through Phenolic CompoundsFelix MüllerJohanna RappAnna-Lena HackerAndré FeithRalf TakorsBastian BlombachIn an oxygenic environment, poorly soluble Fe3+ must be reduced to meet the cellular Fe2+ demand. This study demonstrates that elevated CO2/HCO3− levels accelerate chemical Fe3+ reduction through phenolic compounds, thus increasing intracellular Fe2+ availability. A number of biological environments are characterized by the presence of phenolic compounds and elevated HCO3− levels and include soil habitats and the human body. Fe2+ availability is of particular interest in the latter, as it controls the infectiousness of pathogens. Since the effect postulated here is abiotic, it generally affects the Fe2+ distribution in nature.Iron is a vital mineral for almost all living organisms and has a pivotal role in central metabolism. Despite its great abundance on earth, the accessibility for microorganisms is often limited, because poorly soluble ferric iron (Fe3+) is the predominant oxidation state in an aerobic environment. Hence, the reduction of Fe3+ is of essential importance to meet the cellular demand of ferrous iron (Fe2+) but might become detrimental as excessive amounts of intracellular Fe2+ tend to undergo the cytotoxic Fenton reaction in the presence of hydrogen peroxide. We demonstrate that the complex formation rate of Fe3+ and phenolic compounds like protocatechuic acid was increased by 46% in the presence of HCO3− and thus accelerated the subsequent redox reaction, yielding reduced Fe2+. Consequently, elevated CO2/HCO3− levels increased the intracellular Fe2+ availability, which resulted in at least 50% higher biomass-specific fluorescence of a DtxR-based Corynebacterium glutamicum reporter strain, and stimulated growth. Since the increased Fe2+ availability was attributed to the interaction of HCO3− and chemical iron reduction, the abiotic effect postulated in this study is of general relevance in geochemical and biological environments.https://doi.org/10.1128/mBio.00085-20iron homeostasisiron reductioncarbon dioxidebicarbonatedtxrpathogenscorynebacterium glutamicumiron homeostasis
collection DOAJ
language English
format Article
sources DOAJ
author Felix Müller
Johanna Rapp
Anna-Lena Hacker
André Feith
Ralf Takors
Bastian Blombach
spellingShingle Felix Müller
Johanna Rapp
Anna-Lena Hacker
André Feith
Ralf Takors
Bastian Blombach
CO2/HCO3− Accelerates Iron Reduction through Phenolic Compounds
mBio
iron homeostasis
iron reduction
carbon dioxide
bicarbonate
dtxr
pathogens
corynebacterium glutamicum
iron homeostasis
author_facet Felix Müller
Johanna Rapp
Anna-Lena Hacker
André Feith
Ralf Takors
Bastian Blombach
author_sort Felix Müller
title CO2/HCO3− Accelerates Iron Reduction through Phenolic Compounds
title_short CO2/HCO3− Accelerates Iron Reduction through Phenolic Compounds
title_full CO2/HCO3− Accelerates Iron Reduction through Phenolic Compounds
title_fullStr CO2/HCO3− Accelerates Iron Reduction through Phenolic Compounds
title_full_unstemmed CO2/HCO3− Accelerates Iron Reduction through Phenolic Compounds
title_sort co2/hco3− accelerates iron reduction through phenolic compounds
publisher American Society for Microbiology
series mBio
issn 2150-7511
publishDate 2020-03-01
description In an oxygenic environment, poorly soluble Fe3+ must be reduced to meet the cellular Fe2+ demand. This study demonstrates that elevated CO2/HCO3− levels accelerate chemical Fe3+ reduction through phenolic compounds, thus increasing intracellular Fe2+ availability. A number of biological environments are characterized by the presence of phenolic compounds and elevated HCO3− levels and include soil habitats and the human body. Fe2+ availability is of particular interest in the latter, as it controls the infectiousness of pathogens. Since the effect postulated here is abiotic, it generally affects the Fe2+ distribution in nature.Iron is a vital mineral for almost all living organisms and has a pivotal role in central metabolism. Despite its great abundance on earth, the accessibility for microorganisms is often limited, because poorly soluble ferric iron (Fe3+) is the predominant oxidation state in an aerobic environment. Hence, the reduction of Fe3+ is of essential importance to meet the cellular demand of ferrous iron (Fe2+) but might become detrimental as excessive amounts of intracellular Fe2+ tend to undergo the cytotoxic Fenton reaction in the presence of hydrogen peroxide. We demonstrate that the complex formation rate of Fe3+ and phenolic compounds like protocatechuic acid was increased by 46% in the presence of HCO3− and thus accelerated the subsequent redox reaction, yielding reduced Fe2+. Consequently, elevated CO2/HCO3− levels increased the intracellular Fe2+ availability, which resulted in at least 50% higher biomass-specific fluorescence of a DtxR-based Corynebacterium glutamicum reporter strain, and stimulated growth. Since the increased Fe2+ availability was attributed to the interaction of HCO3− and chemical iron reduction, the abiotic effect postulated in this study is of general relevance in geochemical and biological environments.
topic iron homeostasis
iron reduction
carbon dioxide
bicarbonate
dtxr
pathogens
corynebacterium glutamicum
iron homeostasis
url https://doi.org/10.1128/mBio.00085-20
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