A Model of Aerobic and Anaerobic Metabolism of Hydrogen in the Extremophile Acidithiobacillus ferrooxidans

Abstract

Hydrogen can serve as an electron donor for chemolithotrophic acidophiles, especially in the deep terrestrial subsurface and geothermal ecosystems. Nevertheless, the current knowledge of hydrogen utilization by mesophilic acidophiles is minimal. A multi-omics analysis was applied on Acidithiobacillus ferrooxidans growing on hydrogen, and a respiratory model was proposed. In the model, [NiFe] hydrogenases oxidize hydrogen to two protons and two electrons. The electrons are used to reduce membrane-soluble ubiquinone to ubiquinol. Genetically associated iron-sulfur 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 and reduction of oxygen. Under anaerobic conditions, reduced ubiquinol transfers electrons to outer membrane cytochrome c (ferrireductase) 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 and reduction of ferric iron. The proton gradient generated by hydrogen oxidation maintains the membrane potential and allows the generation of ATP and NADH. These results further clarify the role of extremophiles in biogeochemical processes and their impact on the composition of the deep terrestrial subsurface.

Genomic evolution of the class Acidithiobacillia: deep-branching Proteobacteria living in extreme acidic conditions

“…4A). These functions enable autotrophic growth by dissimilatory H 2 oxidation [82] and anaerobic growth on S 0 coupled to ferric iron reduction [83]. Among Acidithiobacillia taxa, these elements are present only in one other genome, the early branching 'Ambacidithiobacillus sulfuriphilus', which lacks the rus operon for iron oxidation (Fig.…”

Computational structure prediction provides a plausible mechanism for electron transfer by the outer membrane protein Cyc2 from Acidithiobacillus ferrooxidans

“…Cyc2 is the key outer membrane protein in A. ferrooxidans that enables electron transfer from extracellular inorganic materials. 11,63,64 To create a structural model, a modified score function was developed which allows Rosetta comparative modeling protocols to be extended to TMBBs. On a benchmark set of TMBB proteins, RMSDs from native were found to be largest in flexible loop regions (Figure S5c), likely because transmembrane beta sheet spans are conserved among homologs, and the larger conformational diversity within loop regions compared to other secondary structures.…”

“…Cyc2 is the key outer membrane protein in A. ferrooxidans that enables electron transfer from extracellular inorganic materials 11,63,64 . To create a structural model, a modified score function was developed which allows Rosetta comparative modeling protocols to be extended to TMBBs.…”

Computational Structure Prediction Provides a Plausible Mechanism for Electron Transfer by the Outer Membrane Protein Cyc2 fromAcidithiobacillus ferrooxidans

“…Cyc2 is the key outer membrane protein in A. ferrooxidans that enables electron transfer from extracellular inorganic materials (19; 49; 47). To create a structural model, a modified score function was developed which allows Rosetta comparative modeling protocols to be extended to TMBBs.…”