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

Abstract

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.

Authors:
 [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)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Swedish Research Council (SRC)
OSTI Identifier:
1352739
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231; CSP 1505; 2011-5689
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal Issue: 10; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Bagnoud, Alexandre, Chourey, Karuna, Hettich, Robert L., de Bruijn, Ino, Andersson, Anders F., Leupin, Olivier X., Schwyn, Bernhard, and Bernier-Latmani, Rizlan. Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock. United States: N. p., 2016. Web. doi:10.1038/ncomms12770.
Bagnoud, Alexandre, Chourey, Karuna, Hettich, Robert L., de Bruijn, Ino, Andersson, Anders F., Leupin, Olivier X., Schwyn, Bernhard, & Bernier-Latmani, Rizlan. Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock. United States. https://doi.org/10.1038/ncomms12770
Bagnoud, Alexandre, Chourey, Karuna, Hettich, Robert L., de Bruijn, Ino, Andersson, Anders F., Leupin, Olivier X., Schwyn, Bernhard, and Bernier-Latmani, Rizlan. 2016. "Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock". United States. https://doi.org/10.1038/ncomms12770. https://www.osti.gov/servlets/purl/1352739.
@article{osti_1352739,
title = {Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock},
author = {Bagnoud, Alexandre and Chourey, Karuna and Hettich, Robert L. and de Bruijn, Ino and Andersson, Anders F. and Leupin, Olivier X. and Schwyn, Bernhard and Bernier-Latmani, Rizlan},
abstractNote = {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.},
doi = {10.1038/ncomms12770},
url = {https://www.osti.gov/biblio/1352739}, journal = {Nature Communications},
issn = {2041-1723},
number = 10,
volume = 7,
place = {United States},
year = {Fri Oct 14 00:00:00 EDT 2016},
month = {Fri Oct 14 00:00:00 EDT 2016}
}

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Cited by: 64 works
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Works referencing / citing this record:

Function of Biohydrogen Metabolism and Related Microbial Communities in Environmental Bioremediation
journal, February 2019


A shared core microbiome in soda lakes separated by large distances
journal, September 2019


Genome mining- and synthetic biology-enabled production of hypermodified peptides
journal, September 2019


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


Subsurface Microbial Hydrogen Cycling: Natural Occurrence and Implications for Industry
journal, February 2019


Genome mining- and synthetic biology-enabled production of hypermodified peptides
journal, September 2019


Viable cyanobacteria in the deep continental subsurface
journal, October 2018


Ecological and genomic profiling of anaerobic methane-oxidizing archaea in a deep granitic environment
journal, September 2017


Biogeochemical Cycling by a Low-Diversity Microbial Community in Deep Groundwater
journal, September 2018


Metagenomic Insights Into the Microbial Community and Nutrient Cycling in the Western Subarctic Pacific Ocean
journal, April 2018


Fluctuations in populations of subsurface methane oxidizers in coordination with changes in electron acceptor availability
journal, May 2018


A shared core microbiome in soda lakes separated by large distances
journal, September 2019


Metagenomic Insights Into the Microbial Community and Nutrient Cycling in the Western Subarctic Pacific Ocean
journal, April 2018