Examining Pathways of Iron and Sulfur Acquisition, Trafficking, Deployment, and Storage in Mineral-Grown Methanogen Cells

Payne, Devon; Shepard, Eric M.; Spietz, Rachel L.; Steward, Katherine; Brumfield, Sue; Young, Mark; Bothner, Brian; Broderick, William E.; Broderick, Joan B.; Boyd, Eric S.; Galperin, ed., Michael Y.

doi:10.1128/JB.00146-21

Title: Examining Pathways of Iron and Sulfur Acquisition, Trafficking, Deployment, and Storage in Mineral-Grown Methanogen Cells

Journal Article · Wed Sep 08 00:00:00 EDT 2021 · Journal of Bacteriology

DOI:https://doi.org/10.1128/JB.00146-21· OSTI ID:1819238

Payne, Devon ^[1]; Shepard, Eric M. ^[2];

^[1]; Steward, Katherine ^[2]; Brumfield, Sue ^[3]; Young, Mark ^[3];

^[2]; Broderick, William E. ^[2]; Broderick, Joan B. ^[2];

^[1]; Galperin, ed., Michael Y.

Department of Microbiology and Immunology, Montana State University, Bozeman, Montana, USA
Department of Chemistry and Biochemistry, Montana State University, Bozeman, Montana, USA
Department of Plant Sciences, Montana State University, Bozeman, Montana, USA

Methanogens have a high demand for iron (Fe) and sulfur (S); however, little is known of how they acquire, deploy, and store these elements and how this, in turn, affects their physiology. Methanogens were recently shown to reduce pyrite (FeS₂) generating aqueous iron-sulfide (FeS_(aq)) clusters that are likely assimilated as a source of Fe and S. Here, we compare the phenotype of Methanococcus voltae when grown with FeS₂ or ferrous iron (Fe(II)) and sulfide (HS^-). FeS₂-grown cells are 33% smaller yet have 193% more Fe than Fe(II)/HS^--grown cells. Whole cell EPR revealed similar distributions of paramagnetic Fe, although FeS₂-grown cells showed a broad spectral feature attributed to intracellular thioferrate-like nanoparticles. Differential proteomic analyses showed similar expression of core methanogenesis enzymes, indicating that Fe and S source does not substantively alter the energy metabolism of cells. However, a homolog of the Fe(II) transporter FeoB and its putative transcriptional regulator DtxR were up-expressed in FeS₂-grown cells, suggesting that cells sense Fe(II) limitation. Two homologs of IssA, a protein putatively involved in coordinating thioferrate nanoparticles, were also up-expressed in FeS₂-grown cells. We interpret these data to indicate that, in FeS₂-grown cells, DtxR cannot sense Fe(II) and therefore cannot down-regulate FeoB. We suggest this is due to the transport of Fe(II) complexed with sulfide (FeS_(aq)) leading to excess Fe that is sequestered by IssA as a thioferrate-like species. This model provides a framework for the design of targeted experiments aimed at further characterizing Fe acquisition and homeostasis in M. voltae and other methanogens.

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Research Organization:: Montana State Univ., Bozeman, MT (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: SC0020246

OSTI ID:: 1819238

Alternate ID(s):: OSTI ID: 1813462; OSTI ID: 1813862; OSTI ID: 1831429

Journal Information:: Journal of Bacteriology, Journal Name: Journal of Bacteriology Vol. 203 Journal Issue: 19; ISSN 0021-9193

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Title: Examining Pathways of Iron and Sulfur Acquisition, Trafficking, Deployment, and Storage in Mineral-Grown Methanogen Cells

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