Controlling a burn: outer-sphere gating of hydroxylamine oxidation by a distal base in cytochrome P460

Smith, Meghan A.; Majer, Sean H.; Vilbert, Avery C.; Lancaster, Kyle M.

doi:10.1039/C9SC00195F

Title: Controlling a burn: outer-sphere gating of hydroxylamine oxidation by a distal base in cytochrome P460

Journal Article · Wed Mar 27 00:00:00 EDT 2019 · Chemical Science

DOI:https://doi.org/10.1039/C9SC00195F· OSTI ID:1498173

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Department of Chemistry and Chemical Biology, Baker Laboratory, Cornell University, Ithaca, USA

Ammonia oxidizing bacteria (AOB) use the cytotoxic, energetic molecule hydroxylamine (NH₂OH) as a source of reducing equivalents for cellular respiration. Despite disproportionation or violent decomposition being typical outcomes of reactions of NH₂OH with iron, AOB and anammox heme P460 proteins including cytochrome (cyt) P460 and hydroxylamine oxidoreductase (HAO) effect controlled, stepwise oxidation of NH₂OH to nitric oxide (NO). Curiously, a recently characterized cyt P460 variant from the AOB Nitrosomonas sp. AL212 is able to form all intermediates of cyt P460 catalysis, but is nevertheless incompetent for NH₂OH oxidation. We now show via site-directed mutagenesis, activity assays, spectroscopy, and structural biology that this lack of activity is attributable to the absence of a critical basic glutamate residue in the distal pocket above the heme P460 cofactor. This substitution is the only distinguishing characteristic of a protein that is otherwise effectively structurally and spectroscopically identical to an active variant. This highlights and reinforces a fundamental principal of metalloenzymology: metallocofactor inner-sphere geometric and electronic structures are in many cases insufficient for imbuing reactivity; a precisely defined outer coordination sphere contributed by the polypeptide matrix can be the key differentiator between a metalloenzyme and an unreactive metalloprotein.

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Research Organization:: Cornell Univ., Ithaca, NY (United States); Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-06CH11357; SC0013997; DGE-1650441; DMR-1332208; P41 GM103403; S10 RR029205; S10 OD021527; P41 GM103521

OSTI ID:: 1498173

Alternate ID(s):: OSTI ID: 1562700

Journal Information:: Chemical Science, Journal Name: Chemical Science Vol. 10 Journal Issue: 13; ISSN 2041-6520

Publisher:: Royal Society of Chemistry (RSC)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 12 works

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