One-megadalton metalloenzyme complex in Geobacter metallireducens involved in benzene ring reduction beyond the biological redox window

Simona G. Huwiler, Claudia Löffler, Sebastian E. L. Anselmann, Hans-Joachim Stärk, Martin von Bergen, Jennifer Flechsler, Reinhard Rachel, and Matthias Boll
PNAS February 5, 2019 116 (6) 2259-2264; published ahead of print February 5, 2019 https://doi.org/10.1073/pnas.1819636116

  1. Edited by Caroline S. Harwood, University of Washington, Seattle, WA, and approved December 19, 2018 (received for review November 16, 2018)

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Significance

Flavin-based electron bifurcation (FBEB) is a long-hidden mode of energetic coupling in which an endergonic electron transfer process is coupled to an exergonic one. The function of the few FBEB complexes described so far is to achieve ferredoxin reduction at the negative redox limit of the biological redox window. Here, a membrane-associated FBEB complex, isolated and characterized from an anaerobic, aromatic compound-degrading bacterium, achieves a redox reaction beyond this limit possibly by two consecutive FBEB events, with reduced ferredoxin serving as donor. The benzene ring-reducing class II benzoyl-CoA reductase has a [Bam(BC)2DEFGHI]2 composition and represents, with 4 W, 2 Se, 6 FAD, and >50 FeS cofactors, one of the most complex electron transfer machineries in nature.

Abstract

Reversible biological electron transfer usually occurs between redox couples at standard redox potentials ranging from +0.8 to −0.5 V. Dearomatizing benzoyl-CoA reductases (BCRs), key enzymes of the globally relevant microbial degradation of aromatic compounds at anoxic sites, catalyze a biological Birch reduction beyond the negative limit of this redox window. The structurally characterized BamBC subunits of class II BCRs accomplish benzene ring reduction at an active-site tungsten cofactor; however, the mechanism and components involved in the energetic coupling of endergonic benzene ring reduction have remained hypothetical. We present a 1-MDa, membrane-associated, Bam[(BC)2DEFGHI]2 complex from the anaerobic bacterium Geobacter metallireducens harboring 4 tungsten, 4 zinc, 2 selenocysteines, 6 FAD, and >50 FeS cofactors. The results suggest that class II BCRs catalyze electron transfer to the aromatic ring, yielding a cyclic 1,5-dienoyl-CoA via two flavin-based electron bifurcation events. This work expands our knowledge of energetic couplings in biology by high-molecular-mass electron bifurcating machineries.

Footnotes

  • ↵1S.G.H., C.L., and S.E.L.A. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: matthias.boll{at}biologie.uni-freiburg.de.

  • Author contributions: S.G.H. and M.B. designed research; S.G.H., C.L., S.E.L.A., and J.F. performed research; H.-J.S., M.v.B., J.F., and R.R. contributed new reagents/analytic tools; S.G.H., C.L., S.E.L.A., H.-J.S., M.v.B., J.F., and R.R. analyzed data; and S.G.H., S.E.L.A., and M.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1819636116/-/DCSupplemental.

Published under the PNAS license.

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One-megadalton metalloenzyme complex in Geobacter metallireducens involved in benzene ring reduction beyond the biological redox window
Simona G. Huwiler, Claudia Löffler, Sebastian E. L. Anselmann, Hans-Joachim Stärk, Martin von Bergen, Jennifer Flechsler, Reinhard Rachel, Matthias Boll
Proceedings of the National Academy of Sciences Feb 2019, 116 (6) 2259-2264; DOI: 10.1073/pnas.1819636116
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