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

Journal Article · · Nature Communications
DOI:https://doi.org/10.1038/ncomms12770· OSTI ID:1352739
 [1];  [2];  [2]; ORCiD logo [3]; ORCiD logo [4];  [5];  [5];  [1]
  1. Ecole Polytechnique Federale Lausanne (Switzlerland). Environmental Microbiology Lab.
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
  3. Bioinformatics Infrastructure for Life Sciences (BILS), Stockholm (Sweden); KTH Royal Inst. of Technology, Stockholm (Sweden). School of Biotechnology, Division of Gene Technology, Science for Life Lab.
  4. KTH Royal Inst. of Technology, Stockholm (Sweden). School of Biotechnology, Division of Gene Technology, Science for Life Lab.
  5. National Cooperative for the Disposal of Radioactive Waste (Nagra), Wettingen (Switzerland)

A significant fraction (~ 20%) of microbial life is found in the terrestrial deep subsurface, yet the metabolic processes extant in those environments are poorly understood. Here we show that H2, injected into the Opalinus Clay formation in a borehole located 300 meters below the surface, fuels a community of microorganisms with interconnected metabolisms. Metagenomic binning and metaproteomic analysis reveal a complete carbon cycle, driven by autotrophic hydrogen oxidizers. Dead biomass from these organisms is a substrate for a fermenting bacterium that produces acetate as a product. In turn, complete oxidizer heterotrophic sulfate- reducing bacteria utilize acetate and oxidize it to CO2, closing the cycle. This metabolic reconstruction sheds light onto a hydrogen-driven carbon cycle, and a sunlight-independent ecosystem in the deep subsurface.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE Office of Science (SC); Swedish Research Council (SRC)
Grant/Contract Number:
AC05-00OR22725; AC02-05CH11231; CSP 1505; 2011-5689
OSTI ID:
1352739
Journal Information:
Nature Communications, Vol. 7, Issue 10; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 64 works
Citation information provided by
Web of Science

References (42)

An improved method for counting bacteria from sediments and turbid environments by epifluorescence microscopy journal July 2005
Rates of microbial hydrogen oxidation and sulfate reduction in Opalinus Clay rock journal September 2016
Prokaryotes: The unseen majority journal June 1998
Characterization of dissolved organic matter in anoxic rock extracts and in situ pore water of the Opalinus Clay journal December 2007
Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters journal May 1969
Ferrozine---a new spectrophotometric reagent for iron journal June 1970
Environmental Genomics Reveals a Single-Species Ecosystem Deep Within Earth journal October 2008
Microbial Community Analysis of Opalinus Clay Drill Core Samples from the Mont Terri Underground Research Laboratory, Switzerland journal January 2007
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla journal September 2012
A metagenomic window into carbon metabolism at 3 km depth in Precambrian continental crust journal September 2015
Microbial metagenomes from three aquifers in the Fennoscandian shield terrestrial deep biosphere reveal metabolic partitioning among populations journal October 2015
Molecular hydrogen: An abundant energy source for bacterial activity in nuclear waste repositories journal January 2011
Bacterial Physiology and Metabolism book January 1969
Metagenome-assembled genomes uncover a global brackish microbiome journal December 2015
A hydrogen-based subsurface microbial community dominated by methanogens journal January 2002
Physiological and evolutionary potential of microorganisms from the Canterbury Basin subseafloor, a metagenomic approach journal March 2015
Hydrogen Atoms in the Radiolysis of Water journal June 1959
Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field journal April 2004
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal May 2015
Direct Cellular Lysis/Protein Extraction Protocol for Soil Metaproteomics journal December 2010
Hydrogen generation from low-temperature water–rock reactions journal May 2013
Deep subsurface microbial processes journal January 1995
In situ diffusion test of hydrogen gas in the Opalinus Clay journal January 2014
Chemolithotrophy in the continental deep subsurface: Sanford Underground Research Facility (SURF), USA journal November 2014
H alomonas sulfidaeris -dominated microbial community inhabits a 1.8 km-deep subsurface Cambrian Sandstone reservoir : Microbial community inhabits 1.8 km-deep Sandstone journal December 2013
The Mont Terri rock laboratory, a new international research project in a Mesozoic shale formation, in Switzerland journal April 1999
Occurrence, Classification, and Biological Function of Hydrogenases:  An Overview journal October 2007
Occurrence, Classification, and Biological Function of Hydrogenases: An Overview journal December 2007
Microbial life in deep granitic rock journal July 1997
Environmental proteomics reveals early microbial community responses to biostimulation at a uranium- and nitrate-contaminated site journal August 2013
Lithoautotrophic Microbial Ecosystems in Deep Basalt Aquifers journal October 1995
Binning metagenomic contigs by coverage and composition journal September 2014
Taxonomically and functionally diverse microbial communities in deep crystalline rocks of the Fennoscandian shield journal August 2013
Microbial life in deep granitic rock journal March 1997
The evolution of the sulfur cycle journal November 1999
Hydrogen-driven subsurface lithoautotrophic microbial ecosystems (SLiMEs): do they exist and why should we care? journal September 2005
The ecology and biotechnology of sulphate-reducing bacteria journal May 2008
Characterization of dissolved organic matter in anoxic rock extracts and in situ pore water of the Opalinus Clay text January 2007
Slow Microbial Life in the Seabed journal January 2016
Weighing the deep continental biosphere journal September 2013
The Prokaryotes Vol. 6: Proteobacteria: Gamma Subclass reference-book January 2006
The Prokaryotes Vol. 4: Bacteria: Firmicutes, Cyanobacteria reference-book January 2006

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Bacterial and Archaeal Diversity and Abundance in Shallow Subsurface Clay Sediments at Jianghan Plain, China journal October 2020
A shared core microbiome in soda lakes separated by large distances journal September 2019
Erratum for Skennerton et al., “Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea” journal November 2017
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Viable cyanobacteria in the deep continental subsurface journal October 2018
Fifteen years of microbiological investigation in Opalinus Clay at the Mont Terri rock laboratory (Switzerland) book December 2017
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