Aerobic and anaerobic hydrogen respiratory pathways in the extreme acidophile Acidithiobacillus ferrooxidans

ABSTRACT: Hydrogen can be an important source of energy for chemolithotrophic acidophiles, especially in the deep terrestrial subsurface. Nevertheless, the current knowledge of microbial hydrogen utilization in acidic environments is minimal. A multi-omics analysis was applied on Acidithiobacillus ferrooxidans growing aerobically and anaerobically (with ferric iron) on hydrogen as an electron donor, and a respiratory model proposed from the results obtained. In this model, both [NiFe] hydrogenases, cytoplasmic uptake and membrane-bound respiratory, oxidize molecular hydrogen to two protons and two electrons. The electrons are used to reduce membrane-soluble ubiquinone to ubiquinol. Genetically associated [FeS]-binding proteins mediate electron relay from the hydrogenases to the ubiquinone pool. Under aerobic conditions, reduced ubiquinol transfers electrons to either cytochrome aa3 oxidase via cytochrome bc1 complex and cytochrome c4 or the alternate directly to cytochrome bd oxidase, resulting in proton efflux together with the reduction of molecular oxygen to water. Under anaerobic conditions, reduced ubiquinol transfers electrons to outer membrane cytochrome c (ferric iron reductase) via cytochrome bc1 complex and a cascade of electron transporters (cytochrome c4, cytochrome c552, rusticyanin, and high potential iron-sulfur protein), resulting in proton efflux together with the reduction of ferric iron to ferrous iron. The proton gradient generated by molecular hydrogen oxidation maintains the membrane potential and allows the generation of ATP via ATP synthase and NADH via NADH-ubiquinone oxidoreductase. To a lesser extent, NADH can also be generated by another bidirectional cytoplasmic hydrogenase. ATP and NADH are further utilized in the Calvin–Benson–Bassham cycle for inorganic carbon uptake and assimilation. These results further clarify the role of extremophiles in biogeochemical processes and their impact on the composition and features of the deep terrestrial subsurface from the distant past to the present.

INSTRUMENT(S): impact II

ORGANISM(S): Acidithiobacillus Ferrooxidans

TISSUE(S): Cell Suspension Culture

SUBMITTER: Pavel Bouchal  

LAB HEAD: Jiri Kucera

PROVIDER: PXD020361 | Pride | 2020-11-24

REPOSITORIES: Pride