Structural basis for bacterial energy extraction from atmospheric hydrogen.

Sven T Stripp, Chris Greening, Gustav Berggren, Syma Khalid, Kylie A Vincent, Ralf B Schittenhelm, Gregory M Cook, Hannah S Shafaat, Matthew Belousoff, Christopher K Barlow, Rhys Grinter, Ping Huang, Zehui Duan, Ruyu Jia, Princess R Cabotaje, Jack Badley, Moritz Senger, Hari Venugopal, Ashleigh Kropp

Journal: Nature 2023;615(7952):541-547

PMID: 36890228

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Abstract

Diverse aerobic bacteria use atmospheric H as an energy source for growth and survival. This globally significant process regulates the composition of the atmosphere, enhances soil biodiversity and drives primary production in extreme environments. Atmospheric H oxidation is attributed to uncharacterized members of the [NiFe] hydrogenase superfamily. However, it remains unresolved how these enzymes overcome the extraordinary catalytic challenge of oxidizing picomolar levels of H amid ambient levels of the catalytic poison O and how the derived electrons are transferred to the respiratory chain. 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 H to the hydrogenation of the respiratory electron carrier menaquinone. Huc uses narrow hydrophobic gas channels to selectively bind atmospheric H at the expense of O, and 3 [3Fe-4S] clusters modulate the properties of the enzyme so that atmospheric H 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 H oxidation, uncover a mode of energy coupling dependent on long-range quinone transport, and pave the way for the development of catalysts that oxidize H in ambient air.

Address: Department of Microbiology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia. [email protected].; Department of Microbiology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia.; Ramaciotti Centre for Cryo-Electron Microscopy, Monash University, Clayton, Victoria, Australia.; Department of Chemistry, Ångström Laboratory, Uppsala University, Uppsala, Sweden.; Department of Biochemistry, University of Oxford, Oxford, UK.; Department of Chemistry, University of Oxford, Inorganic Chemistry Laboratory, Oxford, UK.; Department of Physics, Experimental Molecular Biophysics, Freie Universität Berlin, Berlin, Germany.; Department of Biochemistry, Monash Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia.; Monash Proteomics and Metabolomics Facility, Monash Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia.; Centre for Electron Microscopy of Membrane Proteins, Monash Institute of Pharmaceutical Sciences, Parkville, Victoria, Australia.; Department of Chemistry and Biochemistry, The Ohio State University, Columbus, OH, USA.; Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealand.; Department of Microbiology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia. [email protected].; Securing Antarctica's Environmental Future, Monash University, Clayton, Victoria, Australia. [email protected].; Centre to Impact AMR, Monash University, Clayton, Victoria, Australia. [email protected].; ARC Research Hub for Carbon Utilisation and Recycling, Monash University, Clayton, Victoria, Australia. [email protected].

DOI: 10.1038/s41586-023-05781-7

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MeSH Terms: Cryoelectron Microscopy, Hydrogen, Hydrogenase, Oxidation-Reduction, Oxygen, Vitamin K 2, Atmosphere, Mycobacterium smegmatis, Hydrogenation