Structure and Spectroscopy of Alkene-Cleaving Dioxygenases Containing an Atypically Coordinated Non-Heme Iron Center
Abstract
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 substratemore »
- Authors:
-
[1];
[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)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Institutes of Health (NIH); Burroughs Wellcome Fund; National Science Foundation (NSF)
- OSTI Identifier:
- 1376251
- Grant/Contract Number:
- AC02-98CH10886; AC02-76SF00515; EY009339; EY020551; CA157735; IK2BX002683; CHE1126268; GM103403; RR029205; P30-EB-009998
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biochemistry
- Additional Journal Information:
- Journal Volume: 56; Journal Issue: 22; Journal ID: ISSN 0006-2960
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; iron; peptides and proteins; surface interactions; crystal structure; phytochemistry
Citation Formats
Sui, Xuewu, Weitz, Andrew C., Farquhar, Erik R., Badiee, Mohsen, Banerjee, Surajit, von Lintig, Johannes, Tochtrop, Gregory P., Palczewski, Krzysztof, Hendrich, Michael P., and Kiser, Philip D. Structure and Spectroscopy of Alkene-Cleaving Dioxygenases Containing an Atypically Coordinated Non-Heme Iron Center. United States: N. p., 2017.
Web. doi:10.1021/acs.biochem.7b00251.
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. Structure and Spectroscopy of Alkene-Cleaving Dioxygenases Containing an Atypically Coordinated Non-Heme Iron Center. United States. https://doi.org/10.1021/acs.biochem.7b00251
Sui, Xuewu, Weitz, Andrew C., Farquhar, Erik R., Badiee, Mohsen, Banerjee, Surajit, von Lintig, Johannes, Tochtrop, Gregory P., Palczewski, Krzysztof, Hendrich, Michael P., and Kiser, Philip D. Thu .
"Structure and Spectroscopy of Alkene-Cleaving Dioxygenases Containing an Atypically Coordinated Non-Heme Iron Center". United States. https://doi.org/10.1021/acs.biochem.7b00251. https://www.osti.gov/servlets/purl/1376251.
@article{osti_1376251,
title = {Structure and Spectroscopy of Alkene-Cleaving Dioxygenases Containing an Atypically Coordinated Non-Heme Iron Center},
author = {Sui, Xuewu and Weitz, Andrew C. and Farquhar, Erik R. and Badiee, Mohsen and Banerjee, Surajit and von Lintig, Johannes and Tochtrop, Gregory P. and Palczewski, Krzysztof and Hendrich, Michael P. and Kiser, Philip D.},
abstractNote = {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.},
doi = {10.1021/acs.biochem.7b00251},
journal = {Biochemistry},
number = 22,
volume = 56,
place = {United States},
year = {Thu May 11 00:00:00 EDT 2017},
month = {Thu May 11 00:00:00 EDT 2017}
}
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