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

Vali, Shaik Waseem; Haja, Dominik K.; Brand, Richard A.; Adams, Michael W. W.; Lindahl, Paul A.

doi:10.1016/j.jbc.2021.100710

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

Journal Article · Fri Jan 01 00:00:00 EST 2021 · Journal of Biological Chemistry

DOI:https://doi.org/10.1016/j.jbc.2021.100710· OSTI ID:1780149

Vali, Shaik Waseem; Haja, Dominik K.;

;

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 Fe^II. 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 Fe^III 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.

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Sponsoring Organization:: 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

Grant/Contract Number:: FG02-95ER20175; GM127021; MCB-1819389; A1170

OSTI ID:: 1780149

Alternate ID(s):: OSTI ID: 1816700

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Vol. 296 Journal Issue: C; ISSN 0021-9258

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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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

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