Structure and Spectroscopy of Alkene-Cleaving Dioxygenases Containing an Atypically Coordinated Non-Heme Iron Center

Sui, Xuewu; Weitz, Andrew C.; Farquhar, Erik R.; Badiee, Mohsen; Banerjee, Surajit; von Lintig, Johannes; Tochtrop, Gregory P.; Palczewski, Krzysztof; Hendrich, Michael P.; Kiser, Philip D.

doi:10.1021/acs.biochem.7b00251

Structure and Spectroscopy of Alkene-Cleaving Dioxygenases Containing an Atypically Coordinated Non-Heme Iron Center

Journal Article · Thu May 11 00:00:00 EDT 2017 · Biochemistry

DOI:https://doi.org/10.1021/acs.biochem.7b00251· OSTI ID:1376251

Sui, Xuewu ^[1]; Weitz, Andrew C. ^[2]; Farquhar, Erik R. ^[3]; Badiee, Mohsen ^[1]; Banerjee, Surajit ^[4]; von Lintig, Johannes ^[1]; Tochtrop, Gregory P. ^[1]; ^[1]; Hendrich, Michael P. ^[2]; ^[5]

Case Western Reserve Univ., Cleveland, OH (United States)
Carnegie Mellon Univ., Pittsburgh, PA (United States)
Brookhaven National Lab. (BNL), Upton, NY (United States); Case Western Reserve Univ., Cleveland, OH (United States)
Argonne National Lab. (ANL), Argonne, IL (United States); Cornell Univ., Ithaca, NY (United States)
Case Western Reserve Univ., Cleveland, OH (United States); Louis Stokes Cleveland VA Medical Center, Cleveland, OH (United States)

Carotenoid cleavage oxygenases (CCOs) are non-heme iron enzymes that catalyze scission of alkene groups in carotenoids and stilbenoids to form biologically important products. CCOs possess a rare four-His iron center whose resting-state structure and interaction with substrates are incompletely understood. Here, we address this knowledge gap through a comprehensive structural and spectroscopic study of three phyletically diverse CCOs. The crystal structure of a fungal stilbenoid-cleaving CCO, CAO1, reveals strong similarity between its iron center and those of carotenoid-cleaving CCOs, but with a markedly different substrate-binding cleft. These enzymes all possess a five-coordinate high-spin Fe(II) center with resting-state Fe–His bond lengths of ~2.15 Å. This ligand set generates an iron environment more electropositive than those of other non-heme iron dioxygenases as observed by Mössbauer isomer shifts. Dioxygen (O₂) does not coordinate iron in the absence of substrate. Substrates bind away (~4.7 Å) from the iron and have little impact on its electronic structure, thus excluding coordination-triggered O₂ binding. However, substrate binding does perturb the spectral properties of CCO Fe–NO derivatives, indicating proximate organic substrate and O₂-binding sites, which might influence Fe–O₂ interactions. Together, these data provide a robust description of the CCO iron center and its interactions with substrates and substrate mimetics that illuminates commonalities as well as subtle and profound structural differences within the CCO family.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: Burroughs Wellcome Fund; National Inst. of Health (NIH); National Science Foundation; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Scientific User Facilities Division

Grant/Contract Number:: AC02-76SF00515; AC02-98CH10886

OSTI ID:: 1376251

Journal Information:: Biochemistry, Journal Name: Biochemistry Journal Issue: 22 Vol. 56; ISSN 0006-2960

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Spectroscopy and crystallography define carotenoid oxygenases as a new subclass of mononuclear non-heme Fe^II enzymes

Journal Article · Mon Mar 24 20:00:00 EDT 2025 · Journal of Biological Chemistry · OSTI ID:2539936

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
crystal structure
iron
peptides and proteins
phytochemistry
surface interactions

Structure and Spectroscopy of Alkene-Cleaving Dioxygenases Containing an Atypically Coordinated Non-Heme Iron Center

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