Structural basis for bacterial energy extraction from atmospheric hydrogen

Rhys Grinter (), Ashleigh Kropp, Hari Venugopal, Moritz Senger, Jack Badley, Princess R. Cabotaje, Ruyu Jia, Zehui Duan, Ping Huang, Sven T. Stripp, Christopher K. Barlow, Matthew Belousoff, Hannah S. Shafaat, Gregory M. Cook, Ralf B. Schittenhelm, Kylie A. Vincent, Syma Khalid, Gustav Berggren and Chris Greening ()
Additional contact information
Rhys Grinter: Monash University
Ashleigh Kropp: Monash University
Hari Venugopal: Monash University
Moritz Senger: Uppsala University
Jack Badley: University of Oxford
Princess R. Cabotaje: Uppsala University
Ruyu Jia: University of Oxford
Zehui Duan: University of Oxford, Inorganic Chemistry Laboratory
Ping Huang: Uppsala University
Sven T. Stripp: Freie Universität Berlin
Christopher K. Barlow: Monash University
Matthew Belousoff: Monash Institute of Pharmaceutical Sciences
Hannah S. Shafaat: The Ohio State University
Gregory M. Cook: University of Otago
Ralf B. Schittenhelm: Monash University
Kylie A. Vincent: University of Oxford, Inorganic Chemistry Laboratory
Syma Khalid: University of Oxford
Gustav Berggren: Uppsala University
Chris Greening: Monash University

Nature, 2023, vol. 615, issue 7952, 541-547

Abstract: Abstract Diverse aerobic bacteria use atmospheric H2 as an energy source for growth and survival1. This globally significant process regulates the composition of the atmosphere, enhances soil biodiversity and drives primary production in extreme environments2,3. Atmospheric H2 oxidation is attributed to uncharacterized members of the [NiFe] hydrogenase superfamily4,5. However, it remains unresolved how these enzymes overcome the extraordinary catalytic challenge of oxidizing picomolar levels of H2 amid ambient levels of the catalytic poison O2 and how the derived electrons are transferred to the respiratory chain1. Here we determined the cryo-electron microscopy structure of the Mycobacterium smegmatis hydrogenase Huc and investigated its mechanism. Huc is a highly efficient oxygen-insensitive enzyme that couples oxidation of atmospheric H2 to the hydrogenation of the respiratory electron carrier menaquinone. Huc uses narrow hydrophobic gas channels to selectively bind atmospheric H2 at the expense of O2, and 3 [3Fe–4S] clusters modulate the properties of the enzyme so that atmospheric H2 oxidation is energetically feasible. The Huc catalytic subunits form an octameric 833 kDa complex around a membrane-associated stalk, which transports and reduces menaquinone 94 Å from the membrane. These findings provide a mechanistic basis for the biogeochemically and ecologically important process of atmospheric H2 oxidation, uncover a mode of energy coupling dependent on long-range quinone transport, and pave the way for the development of catalysts that oxidize H2 in ambient air.

Date: 2023
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DOI: 10.1038/s41586-023-05781-7

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