Nfu facilitates the maturation of iron‐sulfur proteins and participates in virulence in S taphylococcus aureus

Mashruwala, Ameya A.; Pang, Yun Y.; Rosario‐Cruz, Zuelay; Chahal, Harsimranjit K.; Benson, Meredith A.; Mike, Laura A.; Skaar, Eric P.; Torres, Victor J.; Nauseef, William M.; Boyd, Jeffrey M.

doi:10.1111/mmi.12860

Cited by 79Metalloenzymes and iron-sulfur proteinsBacterial Genetics and BiotechnologyAntimicrobial Resistance in Staphylococcus

Nfu facilitates the maturation of iron‐sulfur proteins and participates in virulence in S taphylococcus aureus

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Mashruwala, Ameya A., Pang, Yun Y., Rosario‐Cruz, Zuelay, Chahal, Harsimranjit K., Benson, Meredith A., Mike, Laura A., Skaar, Eric P., Torres, Victor J. +2 more·2015·Molecular Microbiology

DOI 10.1111/mmi.12860PMC PMC4428306

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Abstract

Summary: The acquisition and metabolism of iron ( Fe ) by the human pathogen S taphylococcus aureus is critical for disease progression. S . aureus requires Fe to synthesize inorganic cofactors called iron‐sulfur ( Fe‐S ) clusters, which are required for functional Fe‐S proteins. In this study we investigated the mechanisms utilized by S . aureus to metabolize Fe‐S clusters. We identified that S . aureus utilizes the Suf biosynthetic system to synthesize Fe‐S clusters and we provide genetic evidence suggesting that the suf U and suf B gene products are essential. Additional biochemical and genetic analyses identified Nfu as an Fe‐S cluster carrier, which aids in the maturation of Fe‐S proteins. We find that deletion of the nfu gene negatively impacts staphylococcal physiology and pathogenicity. A nfu mutant accumulates both increased intracellular non‐incorporated Fe and endogenous reactive oxygen species ( ROS ) resulting in DNA damage. In addition, a strain lacking Nfu is sensitive to exogenously supplied ROS and reactive nitrogen species. Congruous with ex vivo findings, a nfu mutant strain is more susceptible to oxidative killing by human polymorphonuclear leukocytes and displays decreased tissue colonization in a murine model of infection. We conclude that Nfu is necessary for staphylococcal pathogenesis and establish Fe‐S cluster metabolism as an attractive antimicrobial target.

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The antibiotic streptonigrin, when combined with intracellular Fe(II) and a reducing agent, promotes killing by causing double-stranded DNA breaks; therefore, increased killing by streptonigrin is correlated with an increased pool of Fe that is not chelated by macromolecules.
“The antibiotic streptonigrin, when combined with intracellular Fe(II) and a reducing agent, promotes killing by causing double-stranded DNA breaks (3,7). Therefore, increased killing by streptonigrin is correlated with an increased pool of Fe that is not chelated by macromolecules.”
From The Staphylococcus aureus non-coding RNA IsrR regulates TCA cycle activity and virulence (2025) · cites this paper as [3]
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S. aureus lacking ftnA displays heightened sensitivity to streptonigrin.
“Previous literature has shown that S. aureus lacking ftnA displays heightened sensitivity to SN (39).”
From The oxidative stress regulator, PerR, is required for staphyloferrin B-mediated iron acquisition in Staphylococcus aureus (2026) · cites this paper as [39]
Staphylococcus aureus strains defective in the acquisition, uptake or proper usage of intracellular Fe have decreased virulence in models of infection.
“Staphylococcus aureus strains defective in the acquisition, uptake or proper usage of intracellular Fe have decreased virulence in models of infection (3–6).”
From The Staphylococcus aureus non-coding RNA IsrR regulates TCA cycle activity and virulence (2025) · cites this paper as [3]

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Two heme-dependent terminal oxidases power Staphylococcus aureus organ-specific colonization of the vertebrate host
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nifU Gene Product from Azotobacter vinelandii Is a Homodimer That Contains Two Identical [2Fe-2S] Clusters
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Molecular characterization of the ferric-uptake regulator, Fur, from Staphylococcus aureus The GenBank accession numbers for the S. aureus fur gene and fhu operon reported in this paper are AF118839 and AF132117, respectively.
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A Proposed Role for the Azotobacter vinelandii NfuA Protein as an Intermediate Iron-Sulfur Cluster Carrier
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SufU Is an Essential Iron-Sulfur Cluster Scaffold Protein in Bacillus subtilis
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An Iron-Sulfur Cluster Is Essential for the Binding of Broken DNA by AddAB-type Helicase-Nucleases
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Monothiol Glutaredoxins Function in Storing and Transporting [Fe2S2] Clusters Assembled on IscU Scaffold Proteins
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Radical S-Adenosylmethionine Enzyme Coproporphyrinogen III Oxidase HemN
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Controlled Expression of nif and isc Iron-Sulfur Protein Maturation Components Reveals Target Specificity and Limited Functional Replacement between the Two Systems
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Arabidopsis thaliana Nfu2 Accommodates [2Fe-2S] or [4Fe-4S] Clusters and Is Competent for in Vitro Maturation of Chloroplast [2Fe-2S] and [4Fe-4S] Cluster-Containing Proteins
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Improved single-copy integration vectors for Staphylococcus aureus
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Phosphatidylinositol-Specific Phospholipase C Contributes to Survival of Staphylococcus aureus USA300 in Human Blood and Neutrophils
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Nitric oxide and peroxynitrite promote complete disruption of the [4Fe-4S] cluster of recombinant human iron regulatory protein 1
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Binding of Azole Antibiotics to Staphylococcus aureus Flavohemoglobin Increases Intracellular Oxidative Stress
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An Intracellular Iron Chelator Pleiotropically Suppresses Enzymatic and Growth Defects of Superoxide Dismutase-Deficient Escherichia coli
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Biogenesis of Iron-Sulfur Clusters in Photosystem I
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The Escherichia coli BtuE Protein Functions as a Resistance Determinant against Reactive Oxygen Species
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Serum iron determination using ferene triazine
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Siderophore-controlled Iron Assimilation in the Enterobacterium Erwinia chrysanthemi
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Bacterial ApbC Protein Has Two Biochemical Activities That Are Required for in Vivo Function
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Salmonella enterica Requires ApbC Function for Growth on Tricarballylate: Evidence of Functional Redundancy between ApbC and IscU
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Generation of Variants in Listeria monocytogenes Continuous-Flow Biofilms Is Dependent on Radical-Induced DNA Damage and RecA-Mediated Repair
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Reconstruction of mreB Expression in Staphylococcus aureus via a Collection of New Integrative Plasmids
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Institute, C.a.L.S. CLSI. Methods for dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approvied Standard-Eighth Edition. CLSA document M07-A8 2009 Clinical and Laboratory Standards Institute Wayne, PA

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Transition Metals and Virulence in Bacteria
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The Suf iron–sulfur cluster biosynthetic system is essential in Staphylococcus aureus, and decreased Suf function results in global metabolic defects and reduced survival in human neutrophils
Roberts, C. A., Al-Tameemi, H. M., Mashruwala, A. A., Rosario-Cruz, Z., Chauhan, U., Sause, W. E., Torres, V. J., Belden, W. J., & Boyd, J. M. (2017) · Infection and Immunity · doi:10.1128/iai.00100-17 · Cited by 84 · see citing works
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Growth and stress tolerance comprise independent metabolic strategies critical for Staphylococcus aureus infection
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The Staphylococcus aureus non-coding RNA IsrR regulates TCA cycle activity and virulence
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“Staphylococcus aureus strains defective in the acquisition, uptake or proper usage of intracellular Fe have decreased virulence in models of infection ( 3–6 ).”
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Fpa (YlaN) is an iron(II) binding protein that functions to relieve Fur-mediated repression of gene expression in Staphylococcus aureus
Boyd, J. M., Ryan Kaler, K., Esquilín-Lebrón, K., Pall, A., Campbell, C. J., Foley, M. E., Rios-Delgado, G., Mustor, E. M., Stephens, T. G., Bovermann, H., et al. (2024) · mBio · doi:10.1128/mbio.02310-24 · Cited by 14 · see citing works
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YlaN is an iron(II) binding protein that functions to relieve Fur-mediated repression of gene expression in Staphylococcus aureus
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The oxidative stress regulator, PerR, is required for staphyloferrin B-mediated iron acquisition in Staphylococcus aureus
Sheikh, A. A., Flannagan, R. S., Nicholson, N. J., Jarycki, N., Fabelurin, R. O., Lewis, I. A., & Heinrichs, D. E. (2026) · Journal of Bacteriology · doi:10.1128/jb.00149-26
“Previous literature has shown that S. aureus lacking ftnA displays heightened sensitivity to SN (39).”

Cloning and Characterization of Rat BAT3 cDNA
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Anthoxanthum Mosaic Virus
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Authors: Mashruwala, A. A., Pang, Y. Y., Rosario‐Cruz, Z., Chahal, H. K., Benson, M. A., Mike, L. A., Skaar, E. P., Torres, V. J., Nauseef, W. M., & Boyd, J. M.
Affiliations: Rutgers, The State University of New Jersey (US)
University of Iowa (US)
NYU Langone Health (US)
Vanderbilt University (US)
Corresponding author: Boyd, Jeffrey M.
ORCID: Mashruwala, Ameya A.
Mike, Laura A.
Skaar, Eric P.
Torres, Victor J.
Nauseef, William M.
Boyd, Jeffrey M.
Venue: Molecular Microbiology
Publisher: Wiley
Published: 2014-12-20
Volume: 95
Issue: 3
Pages: 383-409
ISSN: 0950-382X (ISSN-L)
1365-2958
DOI: 10.1111/mmi.12860
PMC: PMC4428306
OpenAlex: W1873084373
Cited by: 79
References: 147
Citations by year: 2026: 5 · 2025: 10 · 2024: 5 · 2023: 4 · 2022: 4 · 2021: 9 · 2020: 6 · 2019: 12 · 2018: 7 · 2017: 8 · 2016: 6 · 2015: 3
FWCI: 1.87
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Molecular Microbiology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Rutgers University Community Repository (Rutgers University) (submittedVersion)
Funders: National Institutes of Health (AI070958, AI044642, AI069233)
American Heart Association (10PRE3420022)
U.S. Department of Agriculture (NEâˆ’1028)
Topics: Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
Keywords: iron-sulfur proteins, iron-sulfur clusters, Staphylococcus aureus, iron metabolism, virulence, reactive oxygen species, DNA damage, oxidative stress susceptibility, polymorphonuclear leukocytes, tissue colonization, antimicrobial drug targets, SUFU
MeSH terms: Aconitate Hydratase, Animals, Disease Models, Animal, DNA Damage, Multigene Family, Humans, Iron, Iron-Sulfur Proteins, Mutation, Neutrophils, Oxidation-Reduction, Protein Binding, Staphylococcal Infections, Staphylococcus aureus, Sulfur, Virulence, Reactive Oxygen Species, Reactive Nitrogen Species, Mice

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Nfu facilitates the maturation of iron‐sulfur proteins and participates in virulence in S taphylococcus aureus

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