Bacterioferritin of <named-content content-type="genus-species">Magnetospirillum gryphiswaldense</named-content> Is a Heterotetraeicosameric Complex Composed of Functionally Distinct Subunits but Is Not Involved in Magnetite Biomineralization

ABSTRACT The biomineralization pathway of magnetite in magnetotactic bacteria is still poorly understood and a matter of intense debates. In particular, the existence, nature, and location of possible mineral precursors of magnetite are not clear. One possible precursor has been suggested to be ferr...

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Autores principales:	René Uebe, Frederik Ahrens, Jörg Stang, Katharina Jäger, Lars H. Böttger, Christian Schmidt, Berthold F. Matzanke, Dirk Schüler
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	bacterioferritin biomineralization ferritin magnetite oxidative stress prokaryotic organelle Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9505fb837ac54107a361bc03af294b5c
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spelling	oai:doaj.org-article:9505fb837ac54107a361bc03af294b5c2021-11-15T15:55:24ZBacterioferritin of <named-content content-type="genus-species">Magnetospirillum gryphiswaldense</named-content> Is a Heterotetraeicosameric Complex Composed of Functionally Distinct Subunits but Is Not Involved in Magnetite Biomineralization10.1128/mBio.02795-182150-7511https://doaj.org/article/9505fb837ac54107a361bc03af294b5c2019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02795-18https://doaj.org/toc/2150-7511ABSTRACT The biomineralization pathway of magnetite in magnetotactic bacteria is still poorly understood and a matter of intense debates. In particular, the existence, nature, and location of possible mineral precursors of magnetite are not clear. One possible precursor has been suggested to be ferritin-bound ferrihydrite. To clarify its role for magnetite biomineralization, we analyzed and characterized ferritin-like proteins from the magnetotactic alphaproteobacterium Magnetospirillum gryphiswaldense MSR-1, employing genetic, biochemical, and spectroscopic techniques. Transmission Mössbauer spectroscopy of the wild type (WT) and a bacterioferritin (bfr) deletion strain uncovered that the presence of ferrihydrite in cells is coupled to the presence of Bfr. However, bfr and dps deletion mutants, encoding another ferritin-like protein, or even mutants with their codeletion had no impact on magnetite formation in MSR-1. Thus, ferritin-like proteins are not involved in magnetite biomineralization and Bfr-bound ferrihydrite is not a precursor of magnetite biosynthesis. Using transmission electron microscopy and bacterial two-hybrid and electrophoretic methods, we also show that MSR-1 Bfr is an atypical representative of the Bfr subfamily, as it forms tetraeicosameric complexes from two distinct subunits. Furthermore, our analyses revealed that these subunits are functionally divergent, with Bfr1 harboring a ferroxidase activity while only Bfr2 contributes to heme binding. Because of this functional differentiation and the poor formation of homooligomeric Bfr1 complexes, only heterooligomeric Bfr protects cells from oxidative stress in vivo. In summary, our results not only provide novel insights into the biomineralization of magnetite but also reveal the unique properties of so-far-uncharacterized heterooligomeric bacterioferritins. IMPORTANCE Magnetotactic bacteria like Magnetospirillum gryphiswaldense are able to orient along magnetic field lines due to the intracellular formation of magnetite nanoparticles. Biomineralization of magnetite has been suggested to require a yet-unknown ferritin-like ferrihydrite component. Here, we report the identification of a bacterioferritin as the source of ferrihydrite in M. gryphiswaldense and show that, contrary to previous reports, bacterioferritin is not involved in magnetite biomineralization but required for oxidative stress resistance. Additionally, we show that bacterioferritin of M. gryphiswaldense is an unusual member of the bacterioferritin subfamily as it is composed of two functionally distinct subunits. Thus, our findings extend our understanding of the bacterioferritin subfamily and also solve a longstanding question about the magnetite biomineralization pathway.René UebeFrederik AhrensJörg StangKatharina JägerLars H. BöttgerChristian SchmidtBerthold F. MatzankeDirk SchülerAmerican Society for Microbiologyarticlebacterioferritinbiomineralizationferritinmagnetiteoxidative stressprokaryotic organelleMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacterioferritin biomineralization ferritin magnetite oxidative stress prokaryotic organelle Microbiology QR1-502
spellingShingle	bacterioferritin biomineralization ferritin magnetite oxidative stress prokaryotic organelle Microbiology QR1-502 René Uebe Frederik Ahrens Jörg Stang Katharina Jäger Lars H. Böttger Christian Schmidt Berthold F. Matzanke Dirk Schüler Bacterioferritin of <named-content content-type="genus-species">Magnetospirillum gryphiswaldense</named-content> Is a Heterotetraeicosameric Complex Composed of Functionally Distinct Subunits but Is Not Involved in Magnetite Biomineralization
description	ABSTRACT The biomineralization pathway of magnetite in magnetotactic bacteria is still poorly understood and a matter of intense debates. In particular, the existence, nature, and location of possible mineral precursors of magnetite are not clear. One possible precursor has been suggested to be ferritin-bound ferrihydrite. To clarify its role for magnetite biomineralization, we analyzed and characterized ferritin-like proteins from the magnetotactic alphaproteobacterium Magnetospirillum gryphiswaldense MSR-1, employing genetic, biochemical, and spectroscopic techniques. Transmission Mössbauer spectroscopy of the wild type (WT) and a bacterioferritin (bfr) deletion strain uncovered that the presence of ferrihydrite in cells is coupled to the presence of Bfr. However, bfr and dps deletion mutants, encoding another ferritin-like protein, or even mutants with their codeletion had no impact on magnetite formation in MSR-1. Thus, ferritin-like proteins are not involved in magnetite biomineralization and Bfr-bound ferrihydrite is not a precursor of magnetite biosynthesis. Using transmission electron microscopy and bacterial two-hybrid and electrophoretic methods, we also show that MSR-1 Bfr is an atypical representative of the Bfr subfamily, as it forms tetraeicosameric complexes from two distinct subunits. Furthermore, our analyses revealed that these subunits are functionally divergent, with Bfr1 harboring a ferroxidase activity while only Bfr2 contributes to heme binding. Because of this functional differentiation and the poor formation of homooligomeric Bfr1 complexes, only heterooligomeric Bfr protects cells from oxidative stress in vivo. In summary, our results not only provide novel insights into the biomineralization of magnetite but also reveal the unique properties of so-far-uncharacterized heterooligomeric bacterioferritins. IMPORTANCE Magnetotactic bacteria like Magnetospirillum gryphiswaldense are able to orient along magnetic field lines due to the intracellular formation of magnetite nanoparticles. Biomineralization of magnetite has been suggested to require a yet-unknown ferritin-like ferrihydrite component. Here, we report the identification of a bacterioferritin as the source of ferrihydrite in M. gryphiswaldense and show that, contrary to previous reports, bacterioferritin is not involved in magnetite biomineralization but required for oxidative stress resistance. Additionally, we show that bacterioferritin of M. gryphiswaldense is an unusual member of the bacterioferritin subfamily as it is composed of two functionally distinct subunits. Thus, our findings extend our understanding of the bacterioferritin subfamily and also solve a longstanding question about the magnetite biomineralization pathway.
format	article
author	René Uebe Frederik Ahrens Jörg Stang Katharina Jäger Lars H. Böttger Christian Schmidt Berthold F. Matzanke Dirk Schüler
author_facet	René Uebe Frederik Ahrens Jörg Stang Katharina Jäger Lars H. Böttger Christian Schmidt Berthold F. Matzanke Dirk Schüler
author_sort	René Uebe
title	Bacterioferritin of <named-content content-type="genus-species">Magnetospirillum gryphiswaldense</named-content> Is a Heterotetraeicosameric Complex Composed of Functionally Distinct Subunits but Is Not Involved in Magnetite Biomineralization
title_short	Bacterioferritin of <named-content content-type="genus-species">Magnetospirillum gryphiswaldense</named-content> Is a Heterotetraeicosameric Complex Composed of Functionally Distinct Subunits but Is Not Involved in Magnetite Biomineralization
title_full	Bacterioferritin of <named-content content-type="genus-species">Magnetospirillum gryphiswaldense</named-content> Is a Heterotetraeicosameric Complex Composed of Functionally Distinct Subunits but Is Not Involved in Magnetite Biomineralization
title_fullStr	Bacterioferritin of <named-content content-type="genus-species">Magnetospirillum gryphiswaldense</named-content> Is a Heterotetraeicosameric Complex Composed of Functionally Distinct Subunits but Is Not Involved in Magnetite Biomineralization
title_full_unstemmed	Bacterioferritin of <named-content content-type="genus-species">Magnetospirillum gryphiswaldense</named-content> Is a Heterotetraeicosameric Complex Composed of Functionally Distinct Subunits but Is Not Involved in Magnetite Biomineralization
title_sort	bacterioferritin of <named-content content-type="genus-species">magnetospirillum gryphiswaldense</named-content> is a heterotetraeicosameric complex composed of functionally distinct subunits but is not involved in magnetite biomineralization
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/9505fb837ac54107a361bc03af294b5c
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Bacterioferritin of <named-content content-type="genus-species">Magnetospirillum gryphiswaldense</named-content> Is a Heterotetraeicosameric Complex Composed of Functionally Distinct Subunits but Is Not Involved in Magnetite Biomineralization

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