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Title: Biogeochemical Cycling by a Low-Diversity Microbial Community in Deep Groundwater

Abstract

Olkiluoto, an island on the south-west coast of Finland, will host a deep geological repository for the storage of spent nuclear fuel. Microbially induced corrosion from the generation of sulphide is therefore a concern as it could potentially compromise the longevity of the copper waste canisters. Groundwater at Olkiluoto is geochemically stratified with depth and elevated concentrations of sulphide are observed when sulphate-rich and methane-rich groundwaters mix. Particularly high sulphide is observed in methane-rich groundwater from a fracture at 530.6 mbsl, where mixing with sulphate-rich groundwater occurred as the result of an open drill hole connecting two different fractures at different depths. To determine the electron donors fuelling sulphidogenesis, we combined geochemical, isotopic, metagenomic and metaproteomic analyses. This revealed a low diversity microbial community fuelled by hydrogen and organic carbon. Sulphur and carbon isotopes of sulphate and dissolved inorganic carbon, respectively, confirmed that sulphate reduction was ongoing and that CO2 came from the degradation of organic matter. The results demonstrate the impact of introducing sulphate to a methane-rich groundwater with limited electron acceptors and provide insight into extant metabolisms in the terrestrial subsurface.

Authors:
; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1469025
Alternate Identifier(s):
OSTI ID: 1495982
Grant/Contract Number:  
CSP 502935; AC05-00OR22725
Resource Type:
Published Article
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Name: Frontiers in Microbiology Journal Volume: 9; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Media SA
Country of Publication:
Switzerland
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES

Citation Formats

Bell, Emma, Lamminmäki, Tiina, Alneberg, Johannes, Andersson, Anders F., Qian, Chen, Xiong, Weili, Hettich, Robert L., Balmer, Louise, Frutschi, Manon, Sommer, Guillaume, and Bernier-Latmani, Rizlan. Biogeochemical Cycling by a Low-Diversity Microbial Community in Deep Groundwater. Switzerland: N. p., 2018. Web. doi:10.3389/fmicb.2018.02129.
Bell, Emma, Lamminmäki, Tiina, Alneberg, Johannes, Andersson, Anders F., Qian, Chen, Xiong, Weili, Hettich, Robert L., Balmer, Louise, Frutschi, Manon, Sommer, Guillaume, & Bernier-Latmani, Rizlan. Biogeochemical Cycling by a Low-Diversity Microbial Community in Deep Groundwater. Switzerland. doi:https://doi.org/10.3389/fmicb.2018.02129
Bell, Emma, Lamminmäki, Tiina, Alneberg, Johannes, Andersson, Anders F., Qian, Chen, Xiong, Weili, Hettich, Robert L., Balmer, Louise, Frutschi, Manon, Sommer, Guillaume, and Bernier-Latmani, Rizlan. Fri . "Biogeochemical Cycling by a Low-Diversity Microbial Community in Deep Groundwater". Switzerland. doi:https://doi.org/10.3389/fmicb.2018.02129.
@article{osti_1469025,
title = {Biogeochemical Cycling by a Low-Diversity Microbial Community in Deep Groundwater},
author = {Bell, Emma and Lamminmäki, Tiina and Alneberg, Johannes and Andersson, Anders F. and Qian, Chen and Xiong, Weili and Hettich, Robert L. and Balmer, Louise and Frutschi, Manon and Sommer, Guillaume and Bernier-Latmani, Rizlan},
abstractNote = {Olkiluoto, an island on the south-west coast of Finland, will host a deep geological repository for the storage of spent nuclear fuel. Microbially induced corrosion from the generation of sulphide is therefore a concern as it could potentially compromise the longevity of the copper waste canisters. Groundwater at Olkiluoto is geochemically stratified with depth and elevated concentrations of sulphide are observed when sulphate-rich and methane-rich groundwaters mix. Particularly high sulphide is observed in methane-rich groundwater from a fracture at 530.6 mbsl, where mixing with sulphate-rich groundwater occurred as the result of an open drill hole connecting two different fractures at different depths. To determine the electron donors fuelling sulphidogenesis, we combined geochemical, isotopic, metagenomic and metaproteomic analyses. This revealed a low diversity microbial community fuelled by hydrogen and organic carbon. Sulphur and carbon isotopes of sulphate and dissolved inorganic carbon, respectively, confirmed that sulphate reduction was ongoing and that CO2 came from the degradation of organic matter. The results demonstrate the impact of introducing sulphate to a methane-rich groundwater with limited electron acceptors and provide insight into extant metabolisms in the terrestrial subsurface.},
doi = {10.3389/fmicb.2018.02129},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {Switzerland},
year = {2018},
month = {9}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: https://doi.org/10.3389/fmicb.2018.02129

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Works referenced in this record:

Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation
journal, December 2008

  • Ragsdale, Stephen W.; Pierce, Elizabeth
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 12, p. 1873-1898
  • DOI: 10.1016/j.bbapap.2008.08.012

Acetogenesis in the Energy-Starved Deep Biosphere – A Paradox?
journal, January 2012


Response of Deep Subsurface Microbial Community to Different Carbon Sources and Electron Acceptors during ∼2 months Incubation in Microcosms
journal, February 2017


Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters
journal, May 1969


Versatile and open software for comparing large genomes
journal, January 2004

  • Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L.
  • Genome Biology, Vol. 5, Issue 2, R12
  • DOI: 10.1186/gb-2004-5-2-r12

Distribution of culturable microorganisms in Fennoscandian Shield groundwater
journal, February 2002


In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate
journal, January 2007


Manganese- and Iron-Dependent Marine Methane Oxidation
journal, July 2009


Active Microbial Communities Inhabit Sulphate-Methane Interphase in Deep Bedrock Fracture Fluids in Olkiluoto, Finland
journal, January 2015

  • Bomberg, Malin; Nyyssönen, Mari; Pitkänen, Petteri
  • BioMed Research International, Vol. 2015
  • DOI: 10.1155/2015/979530

Rapid Reactivation of Deep Subsurface Microbes in the Presence of C-1 Compounds
journal, February 2015


MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph
journal, January 2015


Archaea catalyze iron-dependent anaerobic oxidation of methane
journal, October 2016

  • Ettwig, Katharina F.; Zhu, Baoli; Speth, Daan
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 45
  • DOI: 10.1073/pnas.1609534113

Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments
journal, March 2017

  • Hernsdorf, Alex W.; Amano, Yuki; Miyakawa, Kazuya
  • The ISME Journal, Vol. 11, Issue 8
  • DOI: 10.1038/ismej.2017.39

Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium Desulfurivibrio alkaliphilus by Sulfide Oxidation with Nitrate
journal, July 2017


Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010

  • Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
  • DOI: 10.1073/pnas.1000080107

Note: Desulfovibrio aespoeensis sp. nov., a mesophilic sulfate-reducing bacterium from deep groundwater at aspo hard rock laboratory, Sweden
journal, January 1998

  • Motamedi, M.; Pedersen, K.
  • International Journal of Systematic Bacteriology, Vol. 48, Issue 1
  • DOI: 10.1099/00207713-48-1-311

BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences
journal, February 2016

  • Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae
  • Journal of Molecular Biology, Vol. 428, Issue 4
  • DOI: 10.1016/j.jmb.2015.11.006

KEGG for integration and interpretation of large-scale molecular data sets
journal, November 2011

  • Kanehisa, M.; Goto, S.; Sato, Y.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr988

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes
journal, February 2009


CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Development of an Enhanced Metaproteomic Approach for Deepening the Microbiome Characterization of the Human Infant Gut
journal, October 2014

  • Xiong, Weili; Giannone, Richard J.; Morowitz, Michael J.
  • Journal of Proteome Research, Vol. 14, Issue 1
  • DOI: 10.1021/pr500936p

Microbial metagenomes from three aquifers in the Fennoscandian shield terrestrial deep biosphere reveal metabolic partitioning among populations
journal, October 2015

  • Wu, Xiaofen; Holmfeldt, Karin; Hubalek, Valerie
  • The ISME Journal, Vol. 10, Issue 5
  • DOI: 10.1038/ismej.2015.185

Viruses in granitic groundwater from 69 to 450 m depth of the Äspö hard rock laboratory, Sweden
journal, February 2008

  • Kyle, Jennifer E.; Eydal, Hallgerd S. C.; Ferris, F. Grant
  • The ISME Journal, Vol. 2, Issue 5
  • DOI: 10.1038/ismej.2008.18

Functional gene surveys from ocean drilling expeditions - a review and perspective
journal, January 2013


Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Evidence for methanogenic Archaea and homoacetogenic Bacteria in deep granitic rock aquifers
journal, July 1997


Sulphate-controlled Diversity of Subterranean Microbial Communities over Depth in Deep Groundwater with Opposing Gradients of Sulphate and Methane
journal, July 2014


Use of an ATP assay to determine viable microbial biomass in Fennoscandian Shield groundwater from depths of 3–1000 m
journal, August 2007


Connectivity to the surface determines diversity patterns in subsurface aquifers of the Fennoscandian shield
journal, March 2016

  • Hubalek, Valerie; Wu, Xiaofen; Eiler, Alexander
  • The ISME Journal, Vol. 10, Issue 10
  • DOI: 10.1038/ismej.2016.36

A Comparative Genomic Analysis of Energy Metabolism in Sulfate Reducing Bacteria and Archaea
journal, January 2011

  • Pereira, Inês A. Cardoso; Ramos, Ana Raquel; Grein, Fabian
  • Frontiers in Microbiology, Vol. 2
  • DOI: 10.3389/fmicb.2011.00069

The Sulfur Oxygenase Reductase from the Mesophilic Bacterium Halothiobacillus neapolitanus Is a Highly Active Thermozyme
journal, December 2011

  • Veith, A.; Botelho, H. M.; Kindinger, F.
  • Journal of Bacteriology, Vol. 194, Issue 3
  • DOI: 10.1128/JB.06531-11

Biogenic processes in crystalline bedrock fractures indicated by carbon isotope signatures of secondary calcite
journal, April 2016


The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

The Ribosomal Database Project: improved alignments and new tools for rRNA analysis
journal, January 2009

  • Cole, J. R.; Wang, Q.; Cardenas, E.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn879

Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock
journal, October 2016

  • Bagnoud, Alexandre; Chourey, Karuna; Hettich, Robert L.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12770

H2-Independent Growth of the Hydrogenotrophic Methanogen Methanococcus maripaludis
journal, February 2013


HydDB: A web tool for hydrogenase classification and analysis
journal, September 2016

  • Søndergaard, Dan; Pedersen, Christian N. S.; Greening, Chris
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep34212

Bacteriophage lytic to Desulfovibrio aespoeensis isolated from deep groundwater
journal, June 2009

  • Eydal, Hallgerd S. C.; Jägevall, Sara; Hermansson, Malte
  • The ISME Journal, Vol. 3, Issue 10
  • DOI: 10.1038/ismej.2009.66

Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage
journal, July 2013

  • Haroon, Mohamed F.; Hu, Shihu; Shi, Ying
  • Nature, Vol. 500, Issue 7464
  • DOI: 10.1038/nature12375

Unifying concepts in anaerobic respiration: Insights from dissimilatory sulfur metabolism
journal, February 2013

  • Grein, Fabian; Ramos, Ana Raquel; Venceslau, Sofia S.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2
  • DOI: 10.1016/J.BBABIO.2012.09.001

Microbial life in deep granitic rock
journal, July 1997


Heterotrophic Communities Supplied by Ancient Organic Carbon Predominate in Deep Fennoscandian Bedrock Fluids
journal, September 2014


Binning metagenomic contigs by coverage and composition
journal, September 2014

  • Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino
  • Nature Methods, Vol. 11, Issue 11
  • DOI: 10.1038/nmeth.3103

Microbial co-occurrence patterns in deep Precambrian bedrock fracture fluids
journal, January 2016

  • Purkamo, Lotta; Bomberg, Malin; Kietäväinen, Riikka
  • Biogeosciences, Vol. 13, Issue 10
  • DOI: 10.5194/bg-13-3091-2016

IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering
journal, August 2009

  • Ma, Ze-Qiang; Dasari, Surendra; Chambers, Matthew C.
  • Journal of Proteome Research, Vol. 8, Issue 8
  • DOI: 10.1021/pr900360j

A review of prokaryotic populations and processes in sub-seafloor sediments, including biosphere:geosphere interactions
journal, June 2014


Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/s0022-2836(05)80360-2

A marine microbial consortium apparently mediating anaerobic oxidation of methane
journal, October 2000

  • Boetius, Antje; Ravenschlag, Katrin; Schubert, Carsten J.
  • Nature, Vol. 407, Issue 6804
  • DOI: 10.1038/35036572

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Tracing the slow growth of anaerobic methane-oxidizing communities by 15N-labelling techniques: 15N-labelling of anaerobic methanotrophs
journal, March 2008


Taxonomically and functionally diverse microbial communities in deep crystalline rocks of the Fennoscandian shield
journal, August 2013

  • Nyyssönen, Mari; Hultman, Jenni; Ahonen, Lasse
  • The ISME Journal, Vol. 8, Issue 1
  • DOI: 10.1038/ismej.2013.125

Continuous-flow isotope ratio mass spectrometric analysis of carbonate minerals: Letter to the Editor
journal, March 2003

  • Spötl, Christoph; Vennemann, Torsten W.
  • Rapid Communications in Mass Spectrometry, Vol. 17, Issue 9
  • DOI: 10.1002/rcm.1010

metaxa 2: improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data
journal, March 2015

  • Bengtsson-Palme, Johan; Hartmann, Martin; Eriksson, Karl Martin
  • Molecular Ecology Resources, Vol. 15, Issue 6
  • DOI: 10.1111/1755-0998.12399

An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers
journal, November 2016

  • Lau, Maggie C. Y.; Kieft, Thomas L.; Kuloyo, Olukayode
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 49
  • DOI: 10.1073/pnas.1612244113

Complete genome sequence of Desulfarculus baarsii type strain (2st14T)
journal, January 2010

  • Sun, Hui; Spring, Stefan; Lapidus, Alla
  • Standards in Genomic Sciences, Vol. 3, Issue 3
  • DOI: 10.4056/sigs.1243258

The MetaCyc database of metabolic pathways and enzymes
journal, October 2017

  • Caspi, Ron; Billington, Richard; Fulcher, Carol A.
  • Nucleic Acids Research, Vol. 46, Issue D1
  • DOI: 10.1093/nar/gkx935

MyriMatch:  Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis
journal, February 2007

  • Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C.
  • Journal of Proteome Research, Vol. 6, Issue 2
  • DOI: 10.1021/pr0604054

FastUniq: A Fast De Novo Duplicates Removal Tool for Paired Short Reads
journal, December 2012


Near-optimal probabilistic RNA-seq quantification
journal, April 2016

  • Bray, Nicolas L.; Pimentel, Harold; Melsted, Páll
  • Nature Biotechnology, Vol. 34, Issue 5
  • DOI: 10.1038/nbt.3519

Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities
journal, January 2005


    Works referencing / citing this record:

    The era of ‘omics’ technologies in the study of microbiologically influenced corrosion
    journal, January 2020