Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock.

Alexandre Bagnoud,Ino De Bruijn,Rizlan Bernier-Latmani,Bernhard Schwyn,Anders F Andersson,Karuna Chourey,Robert L Hettich,Olivier X Leupin

doi:10.1038/ncomms12770

Abstract

The Opalinus Clay formation will host geological nuclear waste repositories in Switzerland. It is expected that gas pressure will build-up due to hydrogen production from steel corrosion, jeopardizing the integrity of the engineered barriers. In an in situ experiment located in the Mont Terri Underground Rock Laboratory, we demonstrate that hydrogen is consumed by microorganisms, fuelling a microbial community. Metagenomic binning and metaproteomic analysis of this deep subsurface community reveals a carbon cycle driven by autotrophic hydrogen oxidizers belonging to novel genera. Necromass is then processed by fermenters, followed by complete oxidation to carbon dioxide by heterotrophic sulfate-reducing bacteria, which closes the cycle. This microbial metabolic web can be integrated in the design of geological repositories to reduce pressure build-up. This study shows that Opalinus Clay harbours the potential for chemolithoautotrophic-based system, and provides a model of microbial carbon cycle in deep subsurface environments where hydrogen and sulfate are present.

Highlights

The Opalinus Clay formation will host geological nuclear waste repositories in Switzerland
Our study demonstrates that Opalinus Clay harbours a microbial community that is able to efficiently oxidize H2, which is beneficial for the safety of deep geological nuclear waste repositories, through the reduction of pressure build-up caused by anoxic steel corrosion
Data indicated that two metagenomic-assembled genomes (MAGs), belonging to families Desulfobulbaceae (c16a) and Rhodospirillaceae (c57), were likely responsible for primary production in this ecosystem: proteomic results for the Desulfobulbaceae MAG confirmed its autotrophic potential by providing evidence for all the proteins in the reductive acetyl-CoA pathway (Fig. 6, Supplementary Table 7); the ability of the Rhodospirillaceae MAG to fix carbon via the Calvin cycle was evidenced by its proteome (Supplementary Data 6)

Summary

Introduction

The Opalinus Clay formation will host geological nuclear waste repositories in Switzerland. Necromass is processed by fermenters, followed by complete oxidation to carbon dioxide by heterotrophic sulfate-reducing bacteria, which closes the cycle This microbial metabolic web can be integrated in the design of geological repositories to reduce pressure build-up. This study shows that Opalinus Clay harbours the potential for chemolithoautotrophic-based system, and provides a model of microbial carbon cycle in deep subsurface environments where hydrogen and sulfate are present. A significant fraction of living microorganisms is found in the deep terrestrial subsurface[1,2], in zones hydrologically disconnected from the Earth’s surface[3] Such microbial communities may not directly rely on sunlight as an energy source, but rather on geogenic reduced compounds, such as hydrogen gas (H2), when buried organic matter is absent[4,5].

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Results

Conclusion