Structural basis for bacterial energy extraction from atmospheric hydrogen

Area of Science:

• Biochemistry
• Microbiology
• Environmental Science

Background:

• Diverse aerobic bacteria utilize atmospheric hydrogen (H₂) for energy, impacting atmospheric composition and soil biodiversity.
• The enzymes responsible for atmospheric H₂ oxidation belong to the [NiFe] hydrogenase superfamily, but their mechanisms remain unclear, especially concerning oxygen sensitivity and electron transfer.

Purpose of the Study:

• To determine the structure and investigate the mechanism of Mycobacterium smegmatis hydrogenase Huc.
• To elucidate how Huc catalyzes the oxidation of low-concentration H₂ in the presence of oxygen and transfers electrons to the respiratory chain.

Main Methods:

• Cryo-electron microscopy was used to determine the structure of Huc.
• Biochemical assays were performed to investigate the enzyme's catalytic mechanism and oxygen insensitivity.

Main Results:

• The cryo-EM structure of Huc revealed an octameric complex with a membrane-associated stalk.
• Huc efficiently oxidizes atmospheric H₂, coupling it to menaquinone reduction, and is insensitive to oxygen due to narrow hydrophobic gas channels.
• Three [3Fe-4S] clusters within Huc modulate its properties for energetically feasible H₂ oxidation.

Conclusions:

• The findings provide a mechanistic basis for atmospheric H₂ oxidation, a critical biogeochemical process.
• Huc utilizes a novel mode of energy coupling involving long-range quinone transport.
• This research opens avenues for developing new catalysts for H₂ oxidation in ambient air.