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

D Barrie Johnson,Jan Lochman,Oldrich Janiczek,Martin Mandl,Sabrina Hedrich,Jiri Kucera,Pavel Bouchal,Kamil Mikulasek,Eva Pakostova

doi:10.3389/fmicb.2020.610836

D Barrie Johnson, Jan Lochman + Show 7 more

Open Access

https://doi.org/10.3389/fmicb.2020.610836

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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.

Highlights

Microbial life in the deep terrestrial subsurface is a subject of considerable interest, as geochemical processes provide a source of energy for the metabolism of chemolithotrophic microbial communities
203 differentially expressed genes (DEGs) and 181 differentially expressed proteins (DEPs) were up-regulated during anaerobic growth on H2, while 168 DEGs and 154 DEPs were down-regulated (Figures 1B,C)
The correlation between the DEGs and DEPs identified by each omics method was modest; 4.8% upregulation and 5.2% downregulation (Figure 1D), respectively

Summary

Introduction

Microbial life in the deep terrestrial subsurface is a subject of considerable interest, as geochemical processes provide a source of energy for the metabolism of chemolithotrophic microbial communities. Microbial processes impact the geochemistry of deep repositories and groundwater reservoirs, affecting the feasibility of resource extraction. Since raw materials, such as metal ores, located close to Earth’s surface are becoming depleted, the exploration of deep-buried (>1 km) mineral deposits is currently focused on the deeper subsurface (Johnson, 2015). Subsurface life is dependent on buried organic matter and geogenic reduced compounds such as hydrogen gas (H2) (Stevens, 1997; Bagnoud et al, 2016). Drill cores taken from the largest known massive sulfide deposit have confirmed the presence of members of hydrogen, methane, iron and sulfur oxidizers, and sulfate-reducers many of which are acidophilic (Puente-Sánchez et al, 2014, 2018)

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