Structure and function of an unusual flavodoxin from the domain Archaea

Prakash, Divya; Iyer, Prashanti R.; Suharti, Suharti; Walters, Karim A.; Santiago-Martinez, Michel Geovanni; Golbeck, John H.; Murakami, Katsuhiko S.; Ferry, James G.

doi:10.1073/pnas.1908578116

Title: Structure and function of an unusual flavodoxin from the domain Archaea

Journal Article · Wed Dec 04 00:00:00 EST 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1908578116· OSTI ID:1577026

^[1]; Iyer, Prashanti R. ^[1]; Suharti, Suharti ^[2]; Walters, Karim A. ^[1]; Santiago-Martinez, Michel Geovanni ^[1];

^[1]; Murakami, Katsuhiko S. ^[1]; Ferry, James G. ^[1]

Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA 16802,
Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA 16802,, Department of Chemistry, State University of Malang, 65145 Malang, East Java, Indonesia

Flavodoxins, electron transfer proteins essential for diverse metabolisms in microbes from the domain Bacteria , are extensively characterized. Remarkably, although genomic annotations of flavodoxins are widespread in microbes from the domain Archaea , none have been isolated and characterized. Herein is described the structural, biochemical, and physiological characterization of an unusual flavodoxin (FldA) from Methanosarcina acetivorans , an acetate-utilizing methane-producing microbe of the domain Archaea . In contrast to all flavodoxins, FldA is homodimeric, markedly less acidic, and stabilizes an anionic semiquinone. The crystal structure reveals an flavin mononucleotide (FMN) binding site unique from all other flavodoxins that provides a rationale for stabilization of the anionic semiquinone and a remarkably low reduction potentials for both the oxidized/semiquinone (−301 mV) and semiquinone/hydroquinone couples (−464 mV). FldA is up-regulated in acetate-grown versus methanol-grown cells and shown here to substitute for ferredoxin in mediating the transfer of low potential electrons from the carbonyl of acetate to the membrane-bound electron transport chain that generates ion gradients driving ATP synthesis. FldA offers potential advantages over ferredoxin by ( i ) sparing iron for abundant iron-sulfur proteins essential for acetotrophic growth and ( ii ) resilience to oxidative damage.

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Research Organization:: Pennsylvania State Univ., University Park, PA (United States); Arizona State Univ., Tempe, AZ (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: FG02-95ER20198 MOD16; SC0010575; FG02-95ER20198; DMR-1332208; GM-103485; R01-GM087350

OSTI ID:: 1577026

Alternate ID(s):: OSTI ID: 1800820

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 116 Journal Issue: 51; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 14 works

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