skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Biological iron-sulfur storage in a thioferrate-protein nanoparticle

Journal Article · · Nature Communications
DOI:https://doi.org/10.1038/ncomms16110· OSTI ID:1393138
 [1];  [2]; ORCiD logo [2];  [2];  [2];  [2];  [3];  [3];  [4];  [5];  [5];  [4];  [3];  [2]
  1. Univ. of Georgia, Athens, GA (United States). Dept. of Chemistry, Dept. of Biochemistry and Molecular Biology
  2. Univ. of Georgia, Athens, GA (United States). Dept. of Biochemistry and Molecular Biology
  3. Univ. of Saskatchewan, Saskatoon, SK (Canada). Dept. of Geological Sciences and Chemistry
  4. Univ. of Georgia, Athens, GA (United States). Dept. of Chemistry
  5. Center for Epigenetics, Grand Rapids, MI (United States). Van Andel Research Inst.

Iron–sulfur clusters are ubiquitous in biology and function in electron transfer and catalysis. We assembled them 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. 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 B 6,400 Fe atoms and B 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.

Research Organization:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)
Grant/Contract Number:
FG05-95ER20175; GM62524
OSTI ID:
1393138
Journal Information:
Nature Communications, Vol. 8; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 14 works
Citation information provided by
Web of Science

References (45)

Sulfur K-Edge X-ray Absorption Spectroscopy of 2Fe−2S Ferredoxin:  Covalency of the Oxidized and Reduced 2Fe Forms and Comparison to Model Complexes journal June 2001
The InterPro protein families database: the classification resource after 15 years journal November 2014
Coordination Chemistry of Microbial Iron Transport journal August 2015
The role of X-ray spectroscopy in understanding the geometric and electronic structure of nitrogenase journal June 2015
Building Fe–S proteins: bacterial strategies journal June 2010
Magnetic properties of potassium dithioferrate: A linear chain antiferromagnet and model compound for the exchange interactions in two-iron ferredoxins journal November 1972
Monothiol Glutaredoxins Function in Storing and Transporting [Fe 2 S 2 ] Clusters Assembled on IscU Scaffold Proteins journal September 2012
Structure, Function, and Formation of Biological Iron-Sulfur Clusters journal June 2005
Crystal Structures of a Piscine Betanodavirus: Mechanisms of Capsid Assembly and Viral Infection journal October 2015
Key Role for Sulfur in Peptide Metabolism and in Regulation of Three Hydrogenases in the Hyperthermophilic Archaeon Pyrococcus furiosus journal January 2001
Iron-Sulfur Clusters: Nature's Modular, Multipurpose Structures journal August 1997
Ligand K-edge X-ray Absorption Spectroscopy and DFT Calculations on [Fe 3 S 4 ] 0,+ Clusters:  Delocalization, Redox, and Effect of the Protein Environment journal December 2004
X-ray Emission Spectroscopy Evidences a Central Carbon in the Nitrogenase Iron-Molybdenum Cofactor journal November 2011
Magnetic susceptibility and ESR study of the covalent-chain antiferromagnets TlFeS 2 and TlFeSe 2 journal December 2001
Microbial metalloproteomes are largely uncharacterized journal July 2010
NifX and NifEN exchange NifB cofactor and the VK-cluster, a newly isolated intermediate of the iron-molybdenum cofactor biosynthetic pathway journal January 2007
Spectroscopic and Functional Characterization of Iron-Bound Forms of Azotobacter vinelandii Nif IscA journal October 2012
Crystal structure of the S-adenosylmethionine-dependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans journal August 2004
Ferritins: furnishing proteins with iron journal January 2016
The antiferromagnetic structures of KFeS2, RbFeS2, KFeSe2, and RbFeSe2 and the correlation between magnetic moments and crystal field calculations journal October 1987
JPred4: a protein secondary structure prediction server journal April 2015
Human Cytosolic Iron Regulatory Protein 1 Contains a Linear Iron−Sulfur Cluster journal October 2001
The nature of green alkaline iron sulfide solutions and the preparation of sodium iron(III) sulfide, NaFeS 2 journal November 1978
Reversible cycling between cysteine persulfide-ligated [2Fe-2S] and cysteine-ligated [4Fe-4S] clusters in the FNR regulatory protein journal September 2012
Measurement of protein using bicinchoninic acid journal October 1985
Ferritin Structure from Mycobacterium tuberculosis: Comparative Study with Homologues Identifies Extended C-Terminus Involved in Ferroxidase Activity journal April 2011
DNA Microarray Analysis of the Hyperthermophilic Archaeon Pyrococcus furiosus: Evidence for a New Type of Sulfur-Reducing Enzyme Complex journal December 2001
Cysteine Is Not the Sulfur Source for Iron-Sulfur Cluster and Methionine Biosynthesis in the Methanogenic Archaeon Methanococcus maripaludis journal August 2010
Oxidation by elemental sulfur and coupling of iron/sulfur complexes. Synthesis and structural characterization of tetrakis(tetraethylammonium) tetrakis(ethanethiolato)hexasulfidotetraferrate, a new Fe/S cluster with a linear Fe4 backbone journal March 1991
Characterization of the selenium-substituted 2[4Fe-4Se] ferredoxin from Clostridium pasteurianum journal September 1982
Polysulfide as a possible substrate for sulfur-reducing bacteria journal November 1993
Magnetic behavior of the KFeS2 journal May 2004
The Nitrogenase FeMo-Cofactor Precursor Formed by NifB Protein: A Diamagnetic Cluster Containing Eight Iron Atoms journal September 2016
Investigation of the Electronic Structure of 2Fe−2S Model Complexes and the Rieske Protein Using Ligand K-Edge X-ray Absorption Spectroscopy journal March 1999
Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C journal June 1986
Formation and Properties of [4Fe-4S] Clusters on the IscU Scaffold Protein journal June 2007
EMAN2: An extensible image processing suite for electron microscopy journal January 2007
Theoretical approaches to x-ray absorption fine structure journal July 2000
IscU as a Scaffold for Iron−Sulfur Cluster Biosynthesis:  Sequential Assembly of [2Fe-2S] and [4Fe-4S] Clusters in IscU journal July 2000
A surface structural model for ferrihydrite I: Sites related to primary charge, molar mass, and mass density journal August 2009
The Elemental Sulfur-Responsive Protein (SipA) from the Hyperthermophilic Archaeon Pyrococcus furiosus Is Regulated by Sulfide in an Iron-Dependent Manner journal August 2010
The Molybdenum Site of Sulfite Oxidase:  A Comparison of Wild-Type and the Cysteine 207 to Serine Mutant Using X-ray Absorption Spectroscopy journal January 1996
The role of mitochondria in cellular iron–sulfur protein biogenesis and iron metabolism journal September 2012
Insights into the Metabolism of Elemental Sulfur by the Hyperthermophilic Archaeon Pyrococcus furiosus: Characterization of a Coenzyme A- Dependent NAD(P)H Sulfur Oxidoreductase journal April 2007
Studies on the Chemical Nature of Clostridial Ferredoxin journal December 1963

Cited By (1)

The bacterial MrpORP is a novel Mrp/NBP35 protein involved in iron-sulfur biogenesis journal January 2019