How a Formate Dehydrogenase Responds to Oxygen: Unexpected O2 Insensitivity of an Enzyme Harboring Tungstopterin, Selenocysteine, and [4Fe–4S] Clusters

Graham, Joel E; Niks, Dimitri; Zane, Grant M; Gui, Qin; Hom, Kellie; Hille, Russ; Wall, Judy D; Raman, C S

doi:10.1021/acscatal.2c00316

Title: How a Formate Dehydrogenase Responds to Oxygen: Unexpected O₂ Insensitivity of an Enzyme Harboring Tungstopterin, Selenocysteine, and [4Fe–4S] Clusters

Journal Article · Wed Aug 10 00:00:00 EDT 2022 · ACS Catalysis

DOI:https://doi.org/10.1021/acscatal.2c00316· OSTI ID:1870560

^[1]; Niks, Dimitri ^[2];

^[3]; Gui, Qin ^[3]; Hom, Kellie ^[1]; Hille, Russ ^[2]; Wall, Judy D ^[3];

^[1]

Univ. of Maryland Baltimore County (UMBC), Baltimore, MD (United States)
Univ. of California, Riverside, CA (United States)
Univ. of Missouri, Columbia, MO (United States)

The reversible two-electron interconversion of formate and CO₂ is catalyzed by both nonmetallo- and metallo-formate dehydrogenases (FDHs). The latter group comprises molybdenum- or tungsten-containing enzymes with the metal coordinated by two equivalents of a pyranopterin cofactor, a cysteinyl or selenocysteinyl (Sec) ligand supplied by the polypeptide, and a catalytically essential terminal sulfido ligand. In addition, these biocatalysts incorporate one or more [4Fe–4S] clusters for facilitating long-distance electron transfer. However, an interesting dichotomy arises when attempting to understand how the metallo-FDHs react with O₂. Whereas existing scholarship portrays these enzymes as being unable to perform in air due to extreme O₂ lability of their metal centers, studies dating as far back as the 1930s emphasize that some of these systems exhibit formate oxidase (FOX) activity, coupling formate oxidation to O₂ reduction. Therefore, to reconcile these conflicting views, we explored context-dependent functional linkages between metallo-FDHs and their cognate electron acceptors within the same organism vis-à-vis catalysis under atmospheric O₂. Here, we report the discovery and characterization of an O₂-insensitive FDH2 from the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough (DvH) that ligates tungsten, Sec, and four [4Fe–4S] clusters. By advancing a robust expression platform for its recombinant production, we eliminate both the requirement of nitrate or azide during purification and reductive activation with thiols and/or formate prior to catalysis. Because the distinctive spectral signatures of formate-reduced DvH-FDH2 remain invariant under anaerobic and aerobic conditions, we benchmarked the enzyme activity in air, identifying CO₂ as the catalytic product. Full reaction progress curve analysis discloses a high catalytic efficiency when probed with a high-potential artificial electron acceptor. Furthermore, we show that DvH-FDH2 enables near-stoichiometric hydrogen peroxide production without superoxide release to achieve O₂ insensitivity. Notably, simultaneous electron transfer to cytochrome c and O₂ reveals that metal-based electron bifurcation is operational in this system. Taken together, our work proves the co-occurrence of redox bifurcated FDH and FOX activities within a metalloenzyme scaffold. These findings set the stage for uncovering previously unknown O₂-insensitive flavin-based electron bifurcation mechanisms, as well as for developing authentic formate/air biofuel cells, engineering O₂-stable FDHs and biohybrid metallocatalysts, and discerning formate bioenergetics of gut microbiota.

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Research Organization:: University of Maryland Baltimore County (UMBC), Baltimore, MD (United States)

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

Grant/Contract Number:: SC0018047

OSTI ID:: 1870560

Report Number(s):: DOE-UMB-0018047

Journal Information:: ACS Catalysis, Vol. 12, Issue 16; Related Information: Supporting Information documentVideo 1; ISSN 2155-5435

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Oxygen-insensitive metal-dependent formate dehydrogenase
Formate oxidase
Tungsten
Pterin
Selenium
Iron-sulfur cluster
Electron Paramagnetic Resonance
13C NMR
Oximetry
Hydrogen peroxide
Electron bifurcation
Sulfate-reducing bacteria
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Title: How a Formate Dehydrogenase Responds to Oxygen: Unexpected O2 Insensitivity of an Enzyme Harboring Tungstopterin, Selenocysteine, and [4Fe–4S] Clusters

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Title: How a Formate Dehydrogenase Responds to Oxygen: Unexpected O₂ Insensitivity of an Enzyme Harboring Tungstopterin, Selenocysteine, and [4Fe–4S] Clusters