Roles of the EnvZ/OmpR Two-Component System and Porins in Iron Acquisition in <italic toggle="yes">Escherichia coli</italic>

ABSTRACT Escherichia coli secretes high-affinity Fe3+ chelators to solubilize and transport chelated Fe3+ via specific outer membrane receptors. In microaerobic and anaerobic growth environments, where the reduced Fe2+ form is predominant, ferrous transport systems fulfill the bacterial need for iro...

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Autores principales:	Henri Gerken, Phu Vuong, Ketaki Soparkar, Rajeev Misra
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	iron homeostasis two-component signal transduction systems porins ferric transport ferrous transport EnvZ/OmpR Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2b6fcdcfa1034a72875ce715332ed59e
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spelling	oai:doaj.org-article:2b6fcdcfa1034a72875ce715332ed59e2021-11-15T15:56:46ZRoles of the EnvZ/OmpR Two-Component System and Porins in Iron Acquisition in <italic toggle="yes">Escherichia coli</italic>10.1128/mBio.01192-202150-7511https://doaj.org/article/2b6fcdcfa1034a72875ce715332ed59e2020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01192-20https://doaj.org/toc/2150-7511ABSTRACT Escherichia coli secretes high-affinity Fe3+ chelators to solubilize and transport chelated Fe3+ via specific outer membrane receptors. In microaerobic and anaerobic growth environments, where the reduced Fe2+ form is predominant, ferrous transport systems fulfill the bacterial need for iron. Expression of genes coding for iron metabolism is controlled by Fur, which when bound to Fe2+ acts as a repressor. Work carried out here shows that the constitutively activated EnvZ/OmpR two-component system, which normally controls expression of the ompC and ompF porin genes, dramatically increases the intracellular pool of accessible iron, as determined by whole-cell electron paramagnetic resonance spectroscopy, by inducing the OmpC/FeoB-mediated ferrous transport pathway. Elevated levels of intracellular iron in turn activated Fur, which inhibited the ferric transport pathway but not the ferrous transport pathway. The data show that the positive effect of constitutively activated EnvZ/OmpR on feoB expression is sufficient to overcome the negative effect of activated Fur on feoB. In a tonB mutant, which lacks functional ferric transport systems, deletion of ompR severely impairs growth on rich medium not supplemented with iron, while the simultaneous deletion of ompC and ompF is not viable. These data, together with the observation of derepression of the Fur regulon in an OmpC mutant, show that the porins play an important role in iron homeostasis. The work presented here also resolves a long-standing paradoxical observation of the effect of certain mutant envZ alleles on iron regulon. IMPORTANCE The work presented here solved a long-standing paradox of the negative effects of certain missense alleles of envZ, which codes for kinase of the EnvZ/OmpR two-component system, on the expression of ferric uptake genes. The data revealed that the constitutive envZ alleles activate the Feo- and OmpC-mediated ferrous uptake pathway to flood the cytoplasm with accessible ferrous iron. This activates the ferric uptake regulator, Fur, which inhibits ferric uptake system but cannot inhibit the feo operon due to the positive effect of activated EnvZ/OmpR. The data also revealed the importance of porins in iron homeostasis.Henri GerkenPhu VuongKetaki SoparkarRajeev MisraAmerican Society for Microbiologyarticleiron homeostasistwo-component signal transduction systemsporinsferric transportferrous transportEnvZ/OmpRMicrobiologyQR1-502ENmBio, Vol 11, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	iron homeostasis two-component signal transduction systems porins ferric transport ferrous transport EnvZ/OmpR Microbiology QR1-502
spellingShingle	iron homeostasis two-component signal transduction systems porins ferric transport ferrous transport EnvZ/OmpR Microbiology QR1-502 Henri Gerken Phu Vuong Ketaki Soparkar Rajeev Misra Roles of the EnvZ/OmpR Two-Component System and Porins in Iron Acquisition in <italic toggle="yes">Escherichia coli</italic>
description	ABSTRACT Escherichia coli secretes high-affinity Fe3+ chelators to solubilize and transport chelated Fe3+ via specific outer membrane receptors. In microaerobic and anaerobic growth environments, where the reduced Fe2+ form is predominant, ferrous transport systems fulfill the bacterial need for iron. Expression of genes coding for iron metabolism is controlled by Fur, which when bound to Fe2+ acts as a repressor. Work carried out here shows that the constitutively activated EnvZ/OmpR two-component system, which normally controls expression of the ompC and ompF porin genes, dramatically increases the intracellular pool of accessible iron, as determined by whole-cell electron paramagnetic resonance spectroscopy, by inducing the OmpC/FeoB-mediated ferrous transport pathway. Elevated levels of intracellular iron in turn activated Fur, which inhibited the ferric transport pathway but not the ferrous transport pathway. The data show that the positive effect of constitutively activated EnvZ/OmpR on feoB expression is sufficient to overcome the negative effect of activated Fur on feoB. In a tonB mutant, which lacks functional ferric transport systems, deletion of ompR severely impairs growth on rich medium not supplemented with iron, while the simultaneous deletion of ompC and ompF is not viable. These data, together with the observation of derepression of the Fur regulon in an OmpC mutant, show that the porins play an important role in iron homeostasis. The work presented here also resolves a long-standing paradoxical observation of the effect of certain mutant envZ alleles on iron regulon. IMPORTANCE The work presented here solved a long-standing paradox of the negative effects of certain missense alleles of envZ, which codes for kinase of the EnvZ/OmpR two-component system, on the expression of ferric uptake genes. The data revealed that the constitutive envZ alleles activate the Feo- and OmpC-mediated ferrous uptake pathway to flood the cytoplasm with accessible ferrous iron. This activates the ferric uptake regulator, Fur, which inhibits ferric uptake system but cannot inhibit the feo operon due to the positive effect of activated EnvZ/OmpR. The data also revealed the importance of porins in iron homeostasis.
format	article
author	Henri Gerken Phu Vuong Ketaki Soparkar Rajeev Misra
author_facet	Henri Gerken Phu Vuong Ketaki Soparkar Rajeev Misra
author_sort	Henri Gerken
title	Roles of the EnvZ/OmpR Two-Component System and Porins in Iron Acquisition in <italic toggle="yes">Escherichia coli</italic>
title_short	Roles of the EnvZ/OmpR Two-Component System and Porins in Iron Acquisition in <italic toggle="yes">Escherichia coli</italic>
title_full	Roles of the EnvZ/OmpR Two-Component System and Porins in Iron Acquisition in <italic toggle="yes">Escherichia coli</italic>
title_fullStr	Roles of the EnvZ/OmpR Two-Component System and Porins in Iron Acquisition in <italic toggle="yes">Escherichia coli</italic>
title_full_unstemmed	Roles of the EnvZ/OmpR Two-Component System and Porins in Iron Acquisition in <italic toggle="yes">Escherichia coli</italic>
title_sort	roles of the envz/ompr two-component system and porins in iron acquisition in <italic toggle="yes">escherichia coli</italic>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/2b6fcdcfa1034a72875ce715332ed59e
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Roles of the EnvZ/OmpR Two-Component System and Porins in Iron Acquisition in <italic toggle="yes">Escherichia coli</italic>

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