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Title: The Pyrococcus furiosus ironome is dominated by [Fe4S4]2+ clusters or thioferrate-like iron depending on the availability of elemental sulfur

Abstract

Pyrococcus furiosus is a hyperthermophilic anaerobic archaeon whose metabolism depends on whether elemental sulfur is (+S0) or is not (-S0) included in growth medium. Under +S0 conditions, expression of respiratory hydrogenase declines while respiratory membrane-bound sulfane reductase and the putative iron-storage protein IssA increase. Our objective was to investigate the iron content of WT and ΔIssA cells under these growth conditions using Mössbauer spectroscopy. WT-S0 cells contained 1 mM Fe, with 85% present as two spectroscopically distinct forms of S = 0 [Fe4S4] 2+ clusters; the remainder was mainly high-spin FeII. WT+S0 cells contained 5 to 9 mM Fe, with 75 to 90% present as magnetically ordered thioferrate-like (TFL) iron nanoparticles. TFL iron was similar to chemically defined thioferrates; both consisted of FeIII ions coordinated by an S4 environment, and both exhibited strong coupling between particles causing high applied fields to have little spectral effect. At high temperatures with magnetic hyperfine interactions abolished, TFL iron exhibited two doublets overlapping those of [Fe4S4] 2+ clusters in -S0 cells. This coincidence arose because of similar coordination environments of TFL iron and cluster iron. The TFL structure was more heterogeneous in the presence of IssA. Presented data suggest that IssA may coordinate insolublemore » iron sulfides as TFL iron, formed as a byproduct of anaerobic sulfur respiration under high iron conditions, which thereby reduces its toxicity to the cell. This was the first Mössbauer characterization of the ironome of an archaeon, and it illustrates differences relative to the iron content of better-studied bacteria such as Escherichia coli.« less

Authors:
; ; ORCiD logo; ORCiD logo; ORCiD logo
Publication Date:
Sponsoring Org.:
USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Institutes of Health (NIH); National Science Foundation (NSF); Robert A. Welch Foundation
OSTI Identifier:
1780149
Alternate Identifier(s):
OSTI ID: 1816700
Grant/Contract Number:  
FG02-95ER20175; GM127021; MCB-1819389; A1170
Resource Type:
Published Article
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Name: Journal of Biological Chemistry Journal Volume: 296 Journal Issue: C; Journal ID: ISSN 0021-9258
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; Mossbauer; electron paramagnetic resonance; magnetically ordered; hyperthermophilic; archaea

Citation Formats

Vali, Shaik Waseem, Haja, Dominik K., Brand, Richard A., Adams, Michael W. W., and Lindahl, Paul A. The Pyrococcus furiosus ironome is dominated by [Fe4S4]2+ clusters or thioferrate-like iron depending on the availability of elemental sulfur. United States: N. p., 2021. Web. doi:10.1016/j.jbc.2021.100710.
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Vali, Shaik Waseem, Haja, Dominik K., Brand, Richard A., Adams, Michael W. W., & Lindahl, Paul A. The Pyrococcus furiosus ironome is dominated by [Fe4S4]2+ clusters or thioferrate-like iron depending on the availability of elemental sulfur. United States. https://doi.org/10.1016/j.jbc.2021.100710
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Vali, Shaik Waseem, Haja, Dominik K., Brand, Richard A., Adams, Michael W. W., and Lindahl, Paul A. Fri . "The Pyrococcus furiosus ironome is dominated by [Fe4S4]2+ clusters or thioferrate-like iron depending on the availability of elemental sulfur". United States. https://doi.org/10.1016/j.jbc.2021.100710.
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@article{osti_1780149,
title = {The Pyrococcus furiosus ironome is dominated by [Fe4S4]2+ clusters or thioferrate-like iron depending on the availability of elemental sulfur},
author = {Vali, Shaik Waseem and Haja, Dominik K. and Brand, Richard A. and Adams, Michael W. W. and Lindahl, Paul A.},
abstractNote = {Pyrococcus furiosus is a hyperthermophilic anaerobic archaeon whose metabolism depends on whether elemental sulfur is (+S0) or is not (-S0) included in growth medium. Under +S0 conditions, expression of respiratory hydrogenase declines while respiratory membrane-bound sulfane reductase and the putative iron-storage protein IssA increase. Our objective was to investigate the iron content of WT and ΔIssA cells under these growth conditions using Mössbauer spectroscopy. WT-S0 cells contained 1 mM Fe, with 85% present as two spectroscopically distinct forms of S = 0 [Fe4S4] 2+ clusters; the remainder was mainly high-spin FeII. WT+S0 cells contained 5 to 9 mM Fe, with 75 to 90% present as magnetically ordered thioferrate-like (TFL) iron nanoparticles. TFL iron was similar to chemically defined thioferrates; both consisted of FeIII ions coordinated by an S4 environment, and both exhibited strong coupling between particles causing high applied fields to have little spectral effect. At high temperatures with magnetic hyperfine interactions abolished, TFL iron exhibited two doublets overlapping those of [Fe4S4] 2+ clusters in -S0 cells. This coincidence arose because of similar coordination environments of TFL iron and cluster iron. The TFL structure was more heterogeneous in the presence of IssA. Presented data suggest that IssA may coordinate insoluble iron sulfides as TFL iron, formed as a byproduct of anaerobic sulfur respiration under high iron conditions, which thereby reduces its toxicity to the cell. This was the first Mössbauer characterization of the ironome of an archaeon, and it illustrates differences relative to the iron content of better-studied bacteria such as Escherichia coli.},
doi = {10.1016/j.jbc.2021.100710},
journal = {Journal of Biological Chemistry},
number = C,
volume = 296,
place = {United States},
year = {Fri Jan 01 00:00:00 EST 2021},
month = {Fri Jan 01 00:00:00 EST 2021}
}
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Works referenced in this record:

Whole-Genome DNA Microarray Analysis of a Hyperthermophile and an Archaeon: Pyrococcus furiosus Grown on Carbohydrates or Peptides
journal, July 2003

Biological iron-sulfur storage in a thioferrate-protein nanoparticle
journal, July 2017

  • Vaccaro, Brian J.; Clarkson, Sonya M.; Holden, James F.
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/ncomms16110

Structure and electron transfer mechanism of pyruvate:ferredoxin oxidoreductase
journal, December 1999

Erratum to “The ‘in-plane’ angular spin distribution in layered systems as obtained by 57Fe Mössbauer spectroscopy” [Nucl. Instr. and Meth. B 196 (2002) 135]
journal, April 2006

  • Kuncser, V.; Keune, W.; Vopsaroiu, M.
  • Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms, Vol. 245, Issue 2
  • DOI: 10.1016/j.nimb.2006.01.022

A highly thermostable ferritin from the hyperthermophilic archaeal anaerobe Pyrococcus furiosus
journal, December 2005

Biophysical Investigation of the Ironome of Human Jurkat Cells and Mitochondria
journal, June 2012

  • Jhurry, Nema D.; Chakrabarti, Mrinmoy; McCormick, Sean P.
  • Biochemistry, Vol. 51, Issue 26
  • DOI: 10.1021/bi300382d

SurR is a master regulator of the primary electron flow pathways in the order Thermococcales: SurR controls electron flow pathways in thermococcales
journal, April 2017

  • Lipscomb, Gina L.; Schut, Gerrit J.; Scott, Robert A.
  • Molecular Microbiology, Vol. 104, Issue 5
  • DOI: 10.1111/mmi.13668

A Computational Framework for Proteome-Wide Pursuit and Prediction of Metalloproteins using ICP-MS and MS/MS Data
journal, February 2011

  • Lancaster, W. Andrew; Praissman, Jeremy L.; Poole, Farris L.
  • BMC Bioinformatics, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2105-12-64

Purification and characterization of pyruvate ferredoxin oxidoreductase from the hyperthermophilic archaeon Pyrococcus furiosus
journal, January 1993

  • Blamey, Jenny M.; Adams, Michael W. W.
  • Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1161, Issue 1, p. 19-27
  • DOI: 10.1016/0167-4838(93)90190-3

SurR: a transcriptional activator and repressor controlling hydrogen and elemental sulphur metabolism in Pyrococcus furiosus
journal, January 2009

Inhibition and stimulation of formation of the ferroxidase center and the iron core in Pyrococcus furiosus ferritin
journal, June 2010

  • Honarmand Ebrahimi, Kourosh; Hagedoorn, Peter-Leon; Hagen, Wilfred R.
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 15, Issue 8
  • DOI: 10.1007/s00775-010-0682-6

Mössbauer and EPR Study of Iron in Vacuoles from Fermenting Saccharomyces cerevisiae
journal, November 2011

  • Cockrell, Allison L.; Holmes-Hampton, Gregory P.; McCormick, Sean P.
  • Biochemistry, Vol. 50, Issue 47
  • DOI: 10.1021/bi2014954

Structure of an Ancient Respiratory System
journal, June 2018

Characterization of Hydrogenase II from the Hyperthermophilic Archaeon Pyrococcus furiosus and Assessment of Its Role in Sulfur Reduction
journal, April 2000

Natural Competence in the Hyperthermophilic Archaeon Pyrococcus furiosus Facilitates Genetic Manipulation: Construction of Markerless Deletions of Genes Encoding the Two Cytoplasmic Hydrogenases
journal, February 2011

  • Lipscomb, Gina L.; Stirrett, Karen; Schut, Gerrit J.
  • Applied and Environmental Microbiology, Vol. 77, Issue 7, p. 2232-2238
  • DOI: 10.1128/AEM.02624-10

Rubrerythrin from the Hyperthermophilic Archaeon Pyrococcus furiosus Is a Rubredoxin-Dependent, Iron-Containing Peroxidase
journal, November 2004

Neutron crystallographic study on rubredoxin from Pyrococcus furiosus by BIX-3, a single-crystal diffractometer for biomacromolecules
journal, July 2004

  • Kurihara, K.; Tanaka, I.; Chatake, T.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 31
  • DOI: 10.1073/pnas.0403807101

Characterization of membrane-bound sulfane reductase: A missing link in the evolution of modern day respiratory complexes
journal, September 2018

  • Wu, Chang-Hao; Schut, Gerrit J.; Poole, Farris L.
  • Journal of Biological Chemistry, Vol. 293, Issue 43
  • DOI: 10.1074/jbc.RA118.005092

Molybdenum Incorporation in Tungsten Aldehyde Oxidoreductase Enzymes from Pyrococcus furiosus
journal, June 2010

  • Sevcenco, Ana-Maria; Bevers, Loes E.; Pinkse, Martijn W. H.
  • Journal of Bacteriology, Vol. 192, Issue 16
  • DOI: 10.1128/JB.00270-10

Deletion Strains Reveal Metabolic Roles for Key Elemental Sulfur-Responsive Proteins in Pyrococcus furiosus
journal, September 2011

  • Bridger, S. L.; Clarkson, S. M.; Stirrett, K.
  • Journal of Bacteriology, Vol. 193, Issue 23
  • DOI: 10.1128/JB.05445-11

Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C
journal, June 1986

  • Fiala, Gerhard; Stetter, Karl O.
  • Archives of Microbiology, Vol. 145, Issue 1, p. 56-61
  • DOI: 10.1007/BF00413027

Mössbauer spectroscopic investigations of the magnetic properties of potassium thioferrate-III
journal, January 1988

Dps-like protein from the hyperthermophilic archaeon Pyrococcus furiosus
journal, May 2006

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

  • Schut, G. J.; Bridger, S. L.; Adams, M. W. W.
  • Journal of Bacteriology, Vol. 189, Issue 12, p. 4431-4441
  • DOI: 10.1128/JB.00031-07

Non-heme iron through the three domains of life
journal, February 2007

  • Andreini, Claudia; Banci, Lucia; Bertini, Ivano
  • Proteins: Structure, Function, and Bioinformatics, Vol. 67, Issue 2
  • DOI: 10.1002/prot.21324

Purification and Characterization of a Membrane-Bound Hydrogenase from the Hyperthermophilic Archaeon Pyrococcus furiosus
journal, June 2000

Structure of the respiratory MBS complex reveals iron-sulfur cluster catalyzed sulfane sulfur reduction in ancient life
journal, November 2020

A novel and remarkably thermostable ferredoxin from the hyperthermophilic archaebacterium Pyrococcus furiosus.
journal, June 1989

Iron Content of Saccharomyces cerevisiae Cells Grown under Iron-Deficient and Iron-Overload Conditions
journal, December 2012

  • Holmes-Hampton, Gregory P.; Jhurry, Nema D.; McCormick, Sean P.
  • Biochemistry, Vol. 52, Issue 1
  • DOI: 10.1021/bi3015339

Structures of the Superoxide Reductase from Pyrococcus furiosus in the Oxidized and Reduced States ,
journal, February 2000

  • Yeh, Andrew P.; Hu, Yonglin; Jenney, Francis E.
  • Biochemistry, Vol. 39, Issue 10
  • DOI: 10.1021/bi992428k

The “in-plane” angular spin distribution in layered systems as obtained by 57Fe Mössbauer spectroscopy
journal, November 2002

  • Kuncser, V.; Keune, W.; Vopsaroiu, M.
  • Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms, Vol. 196, Issue 1-2
  • DOI: 10.1016/S0168-583X(02)01274-0

The Elemental Sulfur-Responsive Protein (SipA) from the Hyperthermophilic Archaeon Pyrococcus furiosus Is Regulated by Sulfide in an Iron-Dependent Manner
journal, August 2010

  • Clarkson, S. M.; Newcomer, E. C.; Young, E. G.
  • Journal of Bacteriology, Vol. 192, Issue 21
  • DOI: 10.1128/JB.00660-10

Anaerobic Microbes: Oxygen Detoxification Without Superoxide Dismutase
journal, October 1999

Key Role for Sulfur in Peptide Metabolism and in Regulation of Three Hydrogenases in the Hyperthermophilic Archaeon Pyrococcus furiosus
journal, January 2001

Characterization of Hydrogenase from the Hyperthermophilic Archaebacterium, Pyrococcus furiosus
journal, March 1989

Evidence that a respiratory shield in Escherichia coli protects a low-molecular-mass FeII pool from O2-dependent oxidation
journal, January 2019

  • Wofford, Joshua D.; Bolaji, Naimah; Dziuba, Nathaniel
  • Journal of Biological Chemistry, Vol. 294, Issue 1
  • DOI: 10.1074/jbc.RA118.005233

Spectroscopic Studies of Pyrococcus furiosus Superoxide Reductase:  Implications for Active-Site Structures and the Catalytic Mechanism
journal, February 2002

  • Clay, Michael D.; Jenney,, Francis E.; Hagedoorn, Peter L.
  • Journal of the American Chemical Society, Vol. 124, Issue 5
  • DOI: 10.1021/ja016889g

Microbial metalloproteomes are largely uncharacterized
journal, July 2010

  • Cvetkovic, Aleksandar; Menon, Angeli Lal; Thorgersen, Michael P.
  • Nature, Vol. 466, Issue 7307
  • DOI: 10.1038/nature09265

Pyruvate ferredoxin oxidoreductase from the hyperthermophilic archaeon, Pyrococcus furiosus, functions as a CoA-dependent pyruvate decarboxylase
journal, September 1997

  • Ma, K.; Hutchins, A.; Sung, S. -J. S.
  • Proceedings of the National Academy of Sciences, Vol. 94, Issue 18
  • DOI: 10.1073/pnas.94.18.9608

Strongly Geometrically Frustrated Magnets
journal, August 1994

Characterization of a Fourth Tungsten-Containing Enzyme from the Hyperthermophilic Archaeon Pyrococcus furiosus
journal, December 2002

Two functionally distinct NADP + -dependent ferredoxin oxidoreductases maintain the primary redox balance of Pyrococcus furiosus
journal, July 2017

  • Nguyen, Diep M. N.; Schut, Gerrit J.; Zadvornyy, Oleg A.
  • Journal of Biological Chemistry, Vol. 292, Issue 35
  • DOI: 10.1074/jbc.M117.794172
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