Biological iron-sulfur storage in a thioferrateprotein nanoparticle

Brian J. Vaccaro; Sonya M. Clarkson; James F. Holden; Dong Woo Lee; Chang Hao Wu; Farris L. Poole; Julien J.H. Cotelesage; Mark J. Hackett; Sahel Mohebbi; Jingchuan Sun; Huilin Li; Michael K. Johnson; Graham N. George; Michael W.W. Adams

doi:10.1038/ncomms16110

Biological iron-sulfur storage in a thioferrateprotein nanoparticle

Brian J. Vaccaro, Sonya M. Clarkson, James F. Holden, Dong Woo Lee, Chang Hao Wu, Farris L. Poole, Julien J.H. Cotelesage, Mark J. Hackett, Sahel Mohebbi, Jingchuan Sun, Huilin Li, Michael K. Johnson, Graham N. George, Michael W.W. Adams

Department of Biotechnology

Research output: Contribution to journal › Article › peer-review

24 Citations (Scopus)

Abstract

Iron-sulfur clusters are ubiquitous in biology and function in electron transfer and catalysis. They are assembled from iron and cysteine sulfur on protein scaffolds. Iron is typically stored as iron oxyhydroxide, ferrihydrite, encapsulated in 12 nm shells of ferritin, which buffers cellular iron availability. Here we have characterized IssA, a protein that stores iron and sulfur as thioferrate, an inorganic anionic polymer previously unknown in biology. IssA forms nanoparticles reaching 300 nm in diameter and is the largest natural metalloprotein complex known. It is a member of a widely distributed protein family that includes nitrogenase maturation factors, NifB and NifX. IssA nanoparticles are visible by electron microscopy as electron-dense bodies in the cytoplasm. Purified nanoparticles appear to be generated from 20 nm units containing ∼6,400 Fe atoms and ∼170 IssA monomers. In support of roles in both iron-sulfur storage and cluster biosynthesis, IssA reconstitutes the [4Fe-4S] cluster in ferredoxin in vitro.

Original language	English
Article number	16110
Journal	Nature communications
Volume	8
DOIs	https://doi.org/10.1038/ncomms16110
Publication status	Published - 2017 Jul 20

Bibliographical note

Funding Information:
This research was supported by a grant from the Division of Chemical Sciences, Geosciences and Biosciences, Office of Basic Energy Sciences of the U.S. Department of Energy (DOE; DE-FG05-95ER20175 to M.W.W.A.) We thank Robert M. Glaeser for providing negative stain electron micrographs and John P. Shields for assistance with whole-cell electron microscopy. Bioinformatic analysis was conducted using the Georgia Advanced Computing Resource Center, a partnership between the University of Georgia's Office of the Vice President for Research and Office of the Vice President for Information Technology. Work at the University of Saskatchewan was supported by the CRC (G.N.G.), NSERC Canada and CIHR (J.J.H.C is a CIHR-THRUST Associate, M.J.H. held a CIHR PDF award and is a CIHR-THRUST fellow). SSRL is supported by the U.S. DOE and NIH. EPR and IssA-mediated apo-Fd reconstitution studies were supported by a grant from the National Institutes of Health (GM62524 to M.K.J.)

All Science Journal Classification (ASJC) codes

General Chemistry
General Biochemistry,Genetics and Molecular Biology
General Physics and Astronomy

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10.1038/ncomms16110

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title = "Biological iron-sulfur storage in a thioferrateprotein nanoparticle",

abstract = "Iron-sulfur clusters are ubiquitous in biology and function in electron transfer and catalysis. They are assembled from iron and cysteine sulfur on protein scaffolds. Iron is typically stored as iron oxyhydroxide, ferrihydrite, encapsulated in 12 nm shells of ferritin, which buffers cellular iron availability. Here we have characterized IssA, a protein that stores iron and sulfur as thioferrate, an inorganic anionic polymer previously unknown in biology. IssA forms nanoparticles reaching 300 nm in diameter and is the largest natural metalloprotein complex known. It is a member of a widely distributed protein family that includes nitrogenase maturation factors, NifB and NifX. IssA nanoparticles are visible by electron microscopy as electron-dense bodies in the cytoplasm. Purified nanoparticles appear to be generated from 20 nm units containing ∼6,400 Fe atoms and ∼170 IssA monomers. In support of roles in both iron-sulfur storage and cluster biosynthesis, IssA reconstitutes the [4Fe-4S] cluster in ferredoxin in vitro.",

author = "Vaccaro, {Brian J.} and Clarkson, {Sonya M.} and Holden, {James F.} and Lee, {Dong Woo} and Wu, {Chang Hao} and Poole, {Farris L.} and Cotelesage, {Julien J.H.} and Hackett, {Mark J.} and Sahel Mohebbi and Jingchuan Sun and Huilin Li and Johnson, {Michael K.} and George, {Graham N.} and Adams, {Michael W.W.}",

note = "Funding Information: This research was supported by a grant from the Division of Chemical Sciences, Geosciences and Biosciences, Office of Basic Energy Sciences of the U.S. Department of Energy (DOE; DE-FG05-95ER20175 to M.W.W.A.) We thank Robert M. Glaeser for providing negative stain electron micrographs and John P. Shields for assistance with whole-cell electron microscopy. Bioinformatic analysis was conducted using the Georgia Advanced Computing Resource Center, a partnership between the University of Georgia's Office of the Vice President for Research and Office of the Vice President for Information Technology. Work at the University of Saskatchewan was supported by the CRC (G.N.G.), NSERC Canada and CIHR (J.J.H.C is a CIHR-THRUST Associate, M.J.H. held a CIHR PDF award and is a CIHR-THRUST fellow). SSRL is supported by the U.S. DOE and NIH. EPR and IssA-mediated apo-Fd reconstitution studies were supported by a grant from the National Institutes of Health (GM62524 to M.K.J.)",

year = "2017",

month = jul,

day = "20",

doi = "10.1038/ncomms16110",

language = "English",

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T1 - Biological iron-sulfur storage in a thioferrateprotein nanoparticle

AU - Vaccaro, Brian J.

AU - Clarkson, Sonya M.

AU - Holden, James F.

AU - Lee, Dong Woo

AU - Wu, Chang Hao

AU - Poole, Farris L.

AU - Cotelesage, Julien J.H.

AU - Hackett, Mark J.

AU - Mohebbi, Sahel

AU - Sun, Jingchuan

AU - Li, Huilin

AU - Johnson, Michael K.

AU - George, Graham N.

AU - Adams, Michael W.W.

N1 - Funding Information: This research was supported by a grant from the Division of Chemical Sciences, Geosciences and Biosciences, Office of Basic Energy Sciences of the U.S. Department of Energy (DOE; DE-FG05-95ER20175 to M.W.W.A.) We thank Robert M. Glaeser for providing negative stain electron micrographs and John P. Shields for assistance with whole-cell electron microscopy. Bioinformatic analysis was conducted using the Georgia Advanced Computing Resource Center, a partnership between the University of Georgia's Office of the Vice President for Research and Office of the Vice President for Information Technology. Work at the University of Saskatchewan was supported by the CRC (G.N.G.), NSERC Canada and CIHR (J.J.H.C is a CIHR-THRUST Associate, M.J.H. held a CIHR PDF award and is a CIHR-THRUST fellow). SSRL is supported by the U.S. DOE and NIH. EPR and IssA-mediated apo-Fd reconstitution studies were supported by a grant from the National Institutes of Health (GM62524 to M.K.J.)

PY - 2017/7/20

Y1 - 2017/7/20

N2 - Iron-sulfur clusters are ubiquitous in biology and function in electron transfer and catalysis. They are assembled from iron and cysteine sulfur on protein scaffolds. Iron is typically stored as iron oxyhydroxide, ferrihydrite, encapsulated in 12 nm shells of ferritin, which buffers cellular iron availability. Here we have characterized IssA, a protein that stores iron and sulfur as thioferrate, an inorganic anionic polymer previously unknown in biology. IssA forms nanoparticles reaching 300 nm in diameter and is the largest natural metalloprotein complex known. It is a member of a widely distributed protein family that includes nitrogenase maturation factors, NifB and NifX. IssA nanoparticles are visible by electron microscopy as electron-dense bodies in the cytoplasm. Purified nanoparticles appear to be generated from 20 nm units containing ∼6,400 Fe atoms and ∼170 IssA monomers. In support of roles in both iron-sulfur storage and cluster biosynthesis, IssA reconstitutes the [4Fe-4S] cluster in ferredoxin in vitro.

AB - Iron-sulfur clusters are ubiquitous in biology and function in electron transfer and catalysis. They are assembled from iron and cysteine sulfur on protein scaffolds. Iron is typically stored as iron oxyhydroxide, ferrihydrite, encapsulated in 12 nm shells of ferritin, which buffers cellular iron availability. Here we have characterized IssA, a protein that stores iron and sulfur as thioferrate, an inorganic anionic polymer previously unknown in biology. IssA forms nanoparticles reaching 300 nm in diameter and is the largest natural metalloprotein complex known. It is a member of a widely distributed protein family that includes nitrogenase maturation factors, NifB and NifX. IssA nanoparticles are visible by electron microscopy as electron-dense bodies in the cytoplasm. Purified nanoparticles appear to be generated from 20 nm units containing ∼6,400 Fe atoms and ∼170 IssA monomers. In support of roles in both iron-sulfur storage and cluster biosynthesis, IssA reconstitutes the [4Fe-4S] cluster in ferredoxin in vitro.

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ER -

Biological iron-sulfur storage in a thioferrateprotein nanoparticle

Abstract

Bibliographical note

All Science Journal Classification (ASJC) codes

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