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

Abstract

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.

Authors:
ORCiD logo; ; ; ; ; ORCiD logo; ;
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1577026
Grant/Contract Number:  
FG02-95ER20198 MOD16; SC0010575
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 51; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

Citation Formats

Prakash, Divya, Iyer, Prashanti R., Suharti, Suharti, Walters, Karim A., Santiago-Martinez, Michel Geovanni, Golbeck, John H., Murakami, Katsuhiko S., and Ferry, James G. Structure and function of an unusual flavodoxin from the domain Archaea. United States: N. p., 2019. Web. doi:10.1073/pnas.1908578116.
Prakash, Divya, Iyer, Prashanti R., Suharti, Suharti, Walters, Karim A., Santiago-Martinez, Michel Geovanni, Golbeck, John H., Murakami, Katsuhiko S., & Ferry, James G. Structure and function of an unusual flavodoxin from the domain Archaea. United States. doi:10.1073/pnas.1908578116.
Prakash, Divya, Iyer, Prashanti R., Suharti, Suharti, Walters, Karim A., Santiago-Martinez, Michel Geovanni, Golbeck, John H., Murakami, Katsuhiko S., and Ferry, James G. Wed . "Structure and function of an unusual flavodoxin from the domain Archaea". United States. doi:10.1073/pnas.1908578116.
@article{osti_1577026,
title = {Structure and function of an unusual flavodoxin from the domain Archaea},
author = {Prakash, Divya and Iyer, Prashanti R. and Suharti, Suharti and Walters, Karim A. and Santiago-Martinez, Michel Geovanni and Golbeck, John H. and Murakami, Katsuhiko S. and Ferry, James G.},
abstractNote = {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.},
doi = {10.1073/pnas.1908578116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 51,
volume = 116,
place = {United States},
year = {2019},
month = {12}
}

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