XFEL Crystal Structures of Peroxidase Compound II

Hanna Kwon; Jaswir Basran; Chinar Pathak; Mahdi Hussain; Sam L Freeman; Alistair Fielding; Anna Bailey; Natalia Stefanou; Hazel A Sparkes; Takehiko Tosha; Keitaro Yamashita; Kunio Hirata; Hironori Murakami; Go Ueno; Hideo Ago; Kensuke Tono; Masaki Yamamoto; Hitomi Sawai; Yoshitsugu Shiro; Hiroshi Sugimoto; Emma Raven; Peter Moody

doi:10.1002/anie.202103010

XFEL Crystal Structures of Peroxidase Compound II

Hanna Kwon, Jaswir Basran, Chinar Pathak, Mahdi Hussain, Sam L Freeman, Alistair Fielding, Anna Bailey, Natalia Stefanou, Hazel A Sparkes, Takehiko Tosha, Keitaro Yamashita, Kunio Hirata, Hironori Murakami, Go Ueno, Hideo Ago, Kensuke Tono, Masaki Yamamoto, Hitomi Sawai, Yoshitsugu Shiro, Hiroshi SugimotoEmma Raven^*, Peter Moody^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

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Abstract

Oxygen activation in all heme enzymes requires the formation of high oxidation states of iron, usually referred to as ferryl heme. There are two known intermediates: Compound I and Compound II. The nature of the ferryl heme-and whether it is an Fe-IV=O or Fe-IV-OH species-is important for controlling reactivity across groups of heme enzymes. The most recent evidence for Compound I indicates that the ferryl heme is an unprotonated Fe-IV=O species. For Compound II, the nature of the ferryl heme is not unambiguously established. Here, we report 1.06 angstrom and 1.50 angstrom crystal structures for Compound II intermediates in cytochrome c peroxidase (CcP) and ascorbate peroxidase (APX), collected using the X-ray free electron laser at SACLA. The structures reveal differences between the two peroxidases. The iron-oxygen bond length in CcP (1.76 angstrom) is notably shorter than in APX (1.87 angstrom). The results indicate that the ferryl species is finely tuned across Compound I and Compound II species in closely related peroxidase enzymes. We propose that this fine-tuning is linked to the functional need for proton delivery to the heme.

Original language	English
Pages (from-to)	14578-14585
Number of pages	8
Journal	Angewandte Chemie - International Edition
Volume	60
Issue number	26
Early online date	19 Jun 2021
DOIs	https://doi.org/10.1002/anie.202103010
Publication status	Published - 21 Jun 2021

Bibliographical note

Funding Information:
This work was supported by BBSRC grants BB/N015940/1 and BB/S020586/1 and travel grants from Diamond Light Source to P.C.E.M. and E.L.R. EPR experiments were carried out in the EPSRC National EPR Research Facility & Service (NS/A000055/1). We acknowledge access to SACLA (experiments (2018A8009, 2019B8009, 2020A8030) and JSPS for support (grant JP20H05452 to H.S. and JP19H05783 to M.Y.).

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© 2021 The Authors. Angewandte Chemie International Edition published by Wiley-VCH GmbH

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Kwon, H., Basran, J., Pathak, C., Hussain, M., Freeman, S. L., Fielding, A., Bailey, A., Stefanou, N., Sparkes, H. A., Tosha, T., Yamashita, K., Hirata, K., Murakami, H., Ueno, G., Ago, H., Tono, K., Yamamoto, M., Sawai, H., Shiro, Y., ... Moody, P. (2021). XFEL Crystal Structures of Peroxidase Compound II. Angewandte Chemie - International Edition, 60(26), 14578-14585. https://doi.org/10.1002/anie.202103010

@article{aecad2f0811642ef902f6b74367310e3,

title = "XFEL Crystal Structures of Peroxidase Compound II",

abstract = "Oxygen activation in all heme enzymes requires the formation of high oxidation states of iron, usually referred to as ferryl heme. There are two known intermediates: Compound I and Compound II. The nature of the ferryl heme-and whether it is an Fe-IV=O or Fe-IV-OH species-is important for controlling reactivity across groups of heme enzymes. The most recent evidence for Compound I indicates that the ferryl heme is an unprotonated Fe-IV=O species. For Compound II, the nature of the ferryl heme is not unambiguously established. Here, we report 1.06 angstrom and 1.50 angstrom crystal structures for Compound II intermediates in cytochrome c peroxidase (CcP) and ascorbate peroxidase (APX), collected using the X-ray free electron laser at SACLA. The structures reveal differences between the two peroxidases. The iron-oxygen bond length in CcP (1.76 angstrom) is notably shorter than in APX (1.87 angstrom). The results indicate that the ferryl species is finely tuned across Compound I and Compound II species in closely related peroxidase enzymes. We propose that this fine-tuning is linked to the functional need for proton delivery to the heme.",

author = "Hanna Kwon and Jaswir Basran and Chinar Pathak and Mahdi Hussain and Freeman, {Sam L} and Alistair Fielding and Anna Bailey and Natalia Stefanou and Sparkes, {Hazel A} and Takehiko Tosha and Keitaro Yamashita and Kunio Hirata and Hironori Murakami and Go Ueno and Hideo Ago and Kensuke Tono and Masaki Yamamoto and Hitomi Sawai and Yoshitsugu Shiro and Hiroshi Sugimoto and Emma Raven and Peter Moody",

note = "Funding Information: This work was supported by BBSRC grants BB/N015940/1 and BB/S020586/1 and travel grants from Diamond Light Source to P.C.E.M. and E.L.R. EPR experiments were carried out in the EPSRC National EPR Research Facility & Service (NS/A000055/1). We acknowledge access to SACLA (experiments (2018A8009, 2019B8009, 2020A8030) and JSPS for support (grant JP20H05452 to H.S. and JP19H05783 to M.Y.). Publisher Copyright: {\textcopyright} 2021 The Authors. Angewandte Chemie International Edition published by Wiley-VCH GmbH",

year = "2021",

month = jun,

day = "21",

doi = "10.1002/anie.202103010",

language = "English",

volume = "60",

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journal = "Angewandte Chemie - International Edition",

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Kwon, H, Basran, J, Pathak, C, Hussain, M, Freeman, SL, Fielding, A, Bailey, A, Stefanou, N, Sparkes, HA, Tosha, T, Yamashita, K, Hirata, K, Murakami, H, Ueno, G, Ago, H, Tono, K, Yamamoto, M, Sawai, H, Shiro, Y, Sugimoto, H, Raven, E & Moody, P 2021, 'XFEL Crystal Structures of Peroxidase Compound II', Angewandte Chemie - International Edition, vol. 60, no. 26, pp. 14578-14585. https://doi.org/10.1002/anie.202103010

TY - JOUR

T1 - XFEL Crystal Structures of Peroxidase Compound II

AU - Kwon, Hanna

AU - Basran, Jaswir

AU - Pathak, Chinar

AU - Hussain, Mahdi

AU - Freeman, Sam L

AU - Fielding, Alistair

AU - Bailey, Anna

AU - Stefanou, Natalia

AU - Sparkes, Hazel A

AU - Tosha, Takehiko

AU - Yamashita, Keitaro

AU - Hirata, Kunio

AU - Murakami, Hironori

AU - Ueno, Go

AU - Ago, Hideo

AU - Tono, Kensuke

AU - Yamamoto, Masaki

AU - Sawai, Hitomi

AU - Shiro, Yoshitsugu

AU - Sugimoto, Hiroshi

AU - Raven, Emma

AU - Moody, Peter

N1 - Funding Information: This work was supported by BBSRC grants BB/N015940/1 and BB/S020586/1 and travel grants from Diamond Light Source to P.C.E.M. and E.L.R. EPR experiments were carried out in the EPSRC National EPR Research Facility & Service (NS/A000055/1). We acknowledge access to SACLA (experiments (2018A8009, 2019B8009, 2020A8030) and JSPS for support (grant JP20H05452 to H.S. and JP19H05783 to M.Y.). Publisher Copyright: © 2021 The Authors. Angewandte Chemie International Edition published by Wiley-VCH GmbH

PY - 2021/6/21

Y1 - 2021/6/21

N2 - Oxygen activation in all heme enzymes requires the formation of high oxidation states of iron, usually referred to as ferryl heme. There are two known intermediates: Compound I and Compound II. The nature of the ferryl heme-and whether it is an Fe-IV=O or Fe-IV-OH species-is important for controlling reactivity across groups of heme enzymes. The most recent evidence for Compound I indicates that the ferryl heme is an unprotonated Fe-IV=O species. For Compound II, the nature of the ferryl heme is not unambiguously established. Here, we report 1.06 angstrom and 1.50 angstrom crystal structures for Compound II intermediates in cytochrome c peroxidase (CcP) and ascorbate peroxidase (APX), collected using the X-ray free electron laser at SACLA. The structures reveal differences between the two peroxidases. The iron-oxygen bond length in CcP (1.76 angstrom) is notably shorter than in APX (1.87 angstrom). The results indicate that the ferryl species is finely tuned across Compound I and Compound II species in closely related peroxidase enzymes. We propose that this fine-tuning is linked to the functional need for proton delivery to the heme.

AB - Oxygen activation in all heme enzymes requires the formation of high oxidation states of iron, usually referred to as ferryl heme. There are two known intermediates: Compound I and Compound II. The nature of the ferryl heme-and whether it is an Fe-IV=O or Fe-IV-OH species-is important for controlling reactivity across groups of heme enzymes. The most recent evidence for Compound I indicates that the ferryl heme is an unprotonated Fe-IV=O species. For Compound II, the nature of the ferryl heme is not unambiguously established. Here, we report 1.06 angstrom and 1.50 angstrom crystal structures for Compound II intermediates in cytochrome c peroxidase (CcP) and ascorbate peroxidase (APX), collected using the X-ray free electron laser at SACLA. The structures reveal differences between the two peroxidases. The iron-oxygen bond length in CcP (1.76 angstrom) is notably shorter than in APX (1.87 angstrom). The results indicate that the ferryl species is finely tuned across Compound I and Compound II species in closely related peroxidase enzymes. We propose that this fine-tuning is linked to the functional need for proton delivery to the heme.

U2 - 10.1002/anie.202103010

DO - 10.1002/anie.202103010

M3 - Article (Academic Journal)

C2 - 33826799

SN - 1433-7851

VL - 60

SP - 14578

EP - 14585

JO - Angewandte Chemie - International Edition

JF - Angewandte Chemie - International Edition

IS - 26

ER -

XFEL Crystal Structures of Peroxidase Compound II

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