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Single-Amino Acid Modifications Reveal Additional Controls on the Proton Pathway of [FeFe]-Hydrogenase

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    Single-Amino Acid Modifications Reveal Additional Controls on the Proton Pathway of [FeFe]-Hydrogenase
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    † Department of Biochemistry & Molecular Biology, Michigan State University, East Lansing, Michigan 48824, United States
    ‡ Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, Michigan 48824, United States
    § Physical Sciences Division, Pacific Northwest National Laboratory, Richland, Washington 99352, United States
    ∥ Department of Fundamental Chemistry, Federal University of Pernambuco, Cidade Universitária,50740-560 Recife, PE, Brazil
    *Address: 510A Biochemistry, Michigan State University, East Lansing, MI 48824-1319. E-mail: [email protected]. Phone: (517) 353-7120;. Fax: (517) 353-9334.
    *Address: Pacific Northwest National Laboratory, P.O. Box 999, Richland, WA 99352. E-mail: [email protected]. Phone: (509) 375-5922.
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    Biochemistry

    Cite this: Biochemistry 2016, 55, 22, 3165–3173
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    https://doi.org/10.1021/acs.biochem.5b01044
    Published May 17, 2016
    Copyright © 2016 American Chemical Society
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    Abstract

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    The proton pathway of [FeFe]-hydrogenase is essential for enzymatic H2 production and oxidation and is composed of four residues and a water molecule. A computational analysis of this pathway in the [FeFe]-hydrogenase from Clostridium pasteurianum revealed that the solvent-exposed residue of the pathway (Glu282) forms hydrogen bonds to two residues outside of the pathway (Arg286 and Ser320), implying that these residues could function in regulating proton transfer. In this study, we show that substituting Arg286 with leucine eliminates hydrogen bonding with Glu282 and results in an ∼3-fold enhancement of H2 production activity when methyl viologen is used as an electron donor, suggesting that Arg286 may help control the rate of proton delivery. In contrast, substitution of Ser320 with alanine reduces the rate ∼5-fold, implying that it either acts as a member of the pathway or influences Glu282 to permit proton transfer. Interestingly, quantum mechanics/molecular mechanics and molecular dynamics calculations indicate that Ser320 does not play a structural role or indirectly influence the barrier for proton movement at the entrance of the channel. Rather, it may act as an additional proton acceptor for the pathway or serve in a regulatory role. While further studies are needed to elucidate the role of Ser320, collectively these data provide insights into the complex proton transport process.

    Copyright © 2016 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.biochem.5b01044.

    • Force field parameters and simulation details utilized for MD, multiple-sequence alignment of selected [FeFe]-hydrogenase protein sequences (Figure S1), computational analysis of the distance between Cα atoms (Figure S2), distances between side chains (Figure S3), average numbers of water molecules around Glu282 in water density maps (Figure S4), and QM/MM simulations of proton transfer from Glu282 to Glu279 in the native form and the S320A variant (Figure S5) (PDF)

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    Biochemistry

    Cite this: Biochemistry 2016, 55, 22, 3165–3173
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.biochem.5b01044
    Published May 17, 2016
    Copyright © 2016 American Chemical Society
    Request reuse permissions

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