Structure and activity of particulate methane monooxygenase arrays in methanotrophs

Yanan Zhu; Christopher W. Koo; C. Keith Cassidy; Matthew C. Spink; Tao Ni; Laura C. Zanetti-Domingues; Benji Bateman; Marisa L. Martin-Fernandez; Juan Shen; Yuewen Sheng; Yun Song; Zhengyi Yang; Amy C. Rosenzweig; Peijun Zhang

doi:10.1038/s41467-022-32752-9

Structure and activity of particulate methane monooxygenase arrays in methanotrophs

Yanan Zhu, Christopher W. Koo, C. Keith Cassidy, Matthew C. Spink, Tao Ni, Laura C. Zanetti-Domingues, Benji Bateman, Marisa L. Martin-Fernandez, Juan Shen, Yuewen Sheng, Yun Song, Zhengyi Yang, Amy C. Rosenzweig^*, Peijun Zhang^*

^*Corresponding author for this work

Molecular Biosciences

Research output: Contribution to journal › Article › peer-review

23 Scopus citations

Abstract

Methane-oxidizing bacteria play a central role in greenhouse gas mitigation and have potential applications in biomanufacturing. Their primary metabolic enzyme, particulate methane monooxygenase (pMMO), is housed in copper-induced intracytoplasmic membranes (ICMs), of which the function and biogenesis are not known. We show by serial cryo-focused ion beam (cryoFIB) milling/scanning electron microscope (SEM) volume imaging and lamellae-based cellular cryo-electron tomography (cryoET) that these ICMs are derived from the inner cell membrane. The pMMO trimer, resolved by cryoET and subtomogram averaging to 4.8 Å in the ICM, forms higher-order hexagonal arrays in intact cells. Array formation correlates with increased enzymatic activity, highlighting the importance of studying the enzyme in its native environment. These findings also demonstrate the power of cryoET to structurally characterize native membrane enzymes in the cellular context.

Original language	English (US)
Article number	5221
Journal	Nature communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-32752-9
State	Published - Dec 2022

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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10.1038/s41467-022-32752-9

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Zhu, Y., Koo, C. W., Cassidy, C. K., Spink, M. C., Ni, T., Zanetti-Domingues, L. C., Bateman, B., Martin-Fernandez, M. L., Shen, J., Sheng, Y., Song, Y., Yang, Z., Rosenzweig, A. C., & Zhang, P. (2022). Structure and activity of particulate methane monooxygenase arrays in methanotrophs. Nature communications, 13(1), Article 5221. https://doi.org/10.1038/s41467-022-32752-9

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title = "Structure and activity of particulate methane monooxygenase arrays in methanotrophs",

abstract = "Methane-oxidizing bacteria play a central role in greenhouse gas mitigation and have potential applications in biomanufacturing. Their primary metabolic enzyme, particulate methane monooxygenase (pMMO), is housed in copper-induced intracytoplasmic membranes (ICMs), of which the function and biogenesis are not known. We show by serial cryo-focused ion beam (cryoFIB) milling/scanning electron microscope (SEM) volume imaging and lamellae-based cellular cryo-electron tomography (cryoET) that these ICMs are derived from the inner cell membrane. The pMMO trimer, resolved by cryoET and subtomogram averaging to 4.8 {\AA} in the ICM, forms higher-order hexagonal arrays in intact cells. Array formation correlates with increased enzymatic activity, highlighting the importance of studying the enzyme in its native environment. These findings also demonstrate the power of cryoET to structurally characterize native membrane enzymes in the cellular context.",

author = "Yanan Zhu and Koo, {Christopher W.} and Cassidy, {C. Keith} and Spink, {Matthew C.} and Tao Ni and Zanetti-Domingues, {Laura C.} and Benji Bateman and Martin-Fernandez, {Marisa L.} and Juan Shen and Yuewen Sheng and Yun Song and Zhengyi Yang and Rosenzweig, {Amy C.} and Peijun Zhang",

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month = dec,

doi = "10.1038/s41467-022-32752-9",

language = "English (US)",

volume = "13",

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AU - Cassidy, C. Keith

AU - Spink, Matthew C.

AU - Ni, Tao

AU - Zanetti-Domingues, Laura C.

AU - Bateman, Benji

AU - Martin-Fernandez, Marisa L.

AU - Shen, Juan

AU - Sheng, Yuewen

AU - Song, Yun

AU - Yang, Zhengyi

AU - Rosenzweig, Amy C.

AU - Zhang, Peijun

PY - 2022/12

Y1 - 2022/12

N2 - Methane-oxidizing bacteria play a central role in greenhouse gas mitigation and have potential applications in biomanufacturing. Their primary metabolic enzyme, particulate methane monooxygenase (pMMO), is housed in copper-induced intracytoplasmic membranes (ICMs), of which the function and biogenesis are not known. We show by serial cryo-focused ion beam (cryoFIB) milling/scanning electron microscope (SEM) volume imaging and lamellae-based cellular cryo-electron tomography (cryoET) that these ICMs are derived from the inner cell membrane. The pMMO trimer, resolved by cryoET and subtomogram averaging to 4.8 Å in the ICM, forms higher-order hexagonal arrays in intact cells. Array formation correlates with increased enzymatic activity, highlighting the importance of studying the enzyme in its native environment. These findings also demonstrate the power of cryoET to structurally characterize native membrane enzymes in the cellular context.

AB - Methane-oxidizing bacteria play a central role in greenhouse gas mitigation and have potential applications in biomanufacturing. Their primary metabolic enzyme, particulate methane monooxygenase (pMMO), is housed in copper-induced intracytoplasmic membranes (ICMs), of which the function and biogenesis are not known. We show by serial cryo-focused ion beam (cryoFIB) milling/scanning electron microscope (SEM) volume imaging and lamellae-based cellular cryo-electron tomography (cryoET) that these ICMs are derived from the inner cell membrane. The pMMO trimer, resolved by cryoET and subtomogram averaging to 4.8 Å in the ICM, forms higher-order hexagonal arrays in intact cells. Array formation correlates with increased enzymatic activity, highlighting the importance of studying the enzyme in its native environment. These findings also demonstrate the power of cryoET to structurally characterize native membrane enzymes in the cellular context.

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Structure and activity of particulate methane monooxygenase arrays in methanotrophs

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pMMO structure from native membranes by cryoET and STA

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Structure and activity of particulate methane monooxygenase arrays in methanotrophs

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pMMO structure from native membranes by cryoET and STA

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