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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 6; pp. 2259 - 2264
• Main Authors: Huwiler, Simona G., Löffler, Claudia, Anselmann, Sebastian E. L., Stärk, Hans-Joachim, von Bergen, Martin, Flechsler, Jennifer, Rachel, Reinhard, Boll, Matthias
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 05.02.2019
• Subjects: Aromatic compounds; Benzene; Benzene - metabolism; Bifurcations; Biodegradation; Biological Sciences; Biological Transport; Catalysis; Cofactors; Coupling (molecular); Couplings; Dinitrocresols - metabolism; Electron transfer; Electron Transport; Electrons; Enzymes - metabolism; Flavin-adenine dinucleotide; Geobacter - metabolism; Geobacter - ultrastructure; Geobacter metallireducens; Hydrocarbons; Iron sulfides; Metalloproteins - metabolism; Metals - metabolism; Microbial degradation; Microorganisms; Multiprotein Complexes - metabolism; Oxidation-Reduction; Oxidoreductases Acting on CH-CH Group Donors - metabolism; Redox properties; Reductases; Reduction; Tungsten; Zinc; electron bifurcation; electron transfer; metalloenzyme; aromatic compound; membrane protein complex
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1819636116

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.