Active anaerobic methane oxidation and sulfur disproportionation in the deep terrestrial subsurface

Bell, Emma; Lamminmäki, Tiina; Alneberg, Johannes; Qian, Chen; Xiong, Weili; Hettich, Robert L.; Frutschi, Manon; Bernier-Latmani, Rizlan

doi:10.1038/s41396-022-01207-w

Title: Active anaerobic methane oxidation and sulfur disproportionation in the deep terrestrial subsurface

Journal Article · Wed Feb 16 00:00:00 EST 2022 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-022-01207-w· OSTI ID:1845369

;

; Alneberg, Johannes; Qian, Chen;

;

; Frutschi, Manon;

Abstract Microbial life is widespread in the terrestrial subsurface and present down to several kilometers depth, but the energy sources that fuel metabolism in deep oligotrophic and anoxic environments remain unclear. In the deep crystalline bedrock of the Fennoscandian Shield at Olkiluoto, Finland, opposing gradients of abiotic methane and ancient seawater-derived sulfate create a terrestrial sulfate-methane transition zone (SMTZ). We used chemical and isotopic data coupled to genome-resolved metaproteogenomics to demonstrate active life and, for the first time, provide direct evidence of active anaerobic oxidation of methane (AOM) in a deep terrestrial bedrock. Proteins from Methanoperedens (formerly ANME-2d) are readily identifiable despite the low abundance (≤1%) of this genus and confirm the occurrence of AOM. This finding is supported by 13C-depleted dissolved inorganic carbon. Proteins from Desulfocapsaceae and Desulfurivibrionaceae, in addition to 34S-enriched sulfate, suggest that these organisms use inorganic sulfur compounds as both electron donor and acceptor. Zerovalent sulfur in the groundwater may derive from abiotic rock interactions, or from a non-obligate syntrophy with Methanoperedens, potentially linking methane and sulfur cycles in Olkiluoto groundwater. Finally, putative episymbionts from the candidate phyla radiation (CPR) and DPANN archaea represented a significant diversity in the groundwater (26/84 genomes) with roles in sulfur and carbon cycling. Our results highlight AOM and sulfur disproportionation as active metabolisms and show that methane and sulfur fuel microbial activity in the deep terrestrial subsurface.

View Journal Article

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; AC05-00OR22725

OSTI ID:: 1845369

Alternate ID(s):: OSTI ID: 1883769

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Vol. 16 Journal Issue: 6; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (102)

Rates of microbial hydrogen oxidation and sulfate reduction in Opalinus Clay rock Bagnoud, Alexandre; Leupin, Olivier; Schwyn, Bernhard Applied Geochemistry, Vol. 72 https://doi.org/10.1016/j.apgeochem.2016.06.011	journal	September 2016
Complete genome sequence of Desulfocapsa sulfexigens, a marine deltaproteobacterium specialized in disproportionating inorganic sulfur compounds Finster, Kai Waldemar; Kjeldsen, Kasper Urup; Kube, Michael Standards in Genomic Sciences, Vol. 8, Issue 1 https://doi.org/10.4056/sigs.3777412	journal	April 2013
TIGRFAMs and Genome Properties: tools for the assignment of molecular function and biological process in prokaryotic genomes Selengut, J. D.; Haft, D. H.; Davidsen, T. Nucleic Acids Research, Vol. 35, Issue Database https://doi.org/10.1093/nar/gkl1043	journal	January 2007
The contribution of the Precambrian continental lithosphere to global H2 production Lollar, Barbara Sherwood; Onstott, T. C.; Lacrampe-Couloume, G. Nature, Vol. 516, Issue 7531 https://doi.org/10.1038/nature14017	journal	December 2014
Molecular mechanism of energy conservation in polysulfide respiration Jormakka, Mika; Yokoyama, Ken; Yano, Takahiro Nature Structural & Molecular Biology, Vol. 15, Issue 7 https://doi.org/10.1038/nsmb.1434	journal	June 2008
Genome-resolved metagenomics reveals site-specific diversity of episymbiotic CPR bacteria and DPANN archaea in groundwater ecosystems He, Christine; Keren, Ray; Whittaker, Michael L. Nature Microbiology, Vol. 6, Issue 3 https://doi.org/10.1038/s41564-020-00840-5	journal	January 2021
Active sulfur cycling in the terrestrial deep subsurface Bell, Emma; Lamminmäki, Tiina; Alneberg, Johannes The ISME Journal, Vol. 14, Issue 5 https://doi.org/10.1038/s41396-020-0602-x	journal	February 2020
High precision NMR structure of YhhP, a novel Escherichia coli protein implicated in cell division Katoh, Etsuko; Hatta, Tomohisa; Shindo, Heisaburo Journal of Molecular Biology, Vol. 304, Issue 2 https://doi.org/10.1006/jmbi.2000.4170	journal	November 2000
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla Wrighton, K. C.; Thomas, B. C.; Sharon, I. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224041	journal	September 2012
Disproportionation of inorganic sulfur compounds by a novel autotrophic bacterium belonging to Nitrospirota Umezawa, Kazuhiro; Kojima, Hisaya; Kato, Yukako Systematic and Applied Microbiology, Vol. 43, Issue 5 https://doi.org/10.1016/j.syapm.2020.126110	journal	September 2020
Active Microbial Communities Inhabit Sulphate-Methane Interphase in Deep Bedrock Fracture Fluids in Olkiluoto, Finland Bomberg, Malin; Nyyssönen, Mari; Pitkänen, Petteri BioMed Research International, Vol. 2015 https://doi.org/10.1155/2015/979530	journal	January 2015
Targeted isolation and cultivation of uncultivated bacteria by reverse genomics Cross, Karissa L.; Campbell, James H.; Balachandran, Manasi Nature Biotechnology, Vol. 37, Issue 11 https://doi.org/10.1038/s41587-019-0260-6	journal	September 2019
GToTree: a user-friendly workflow for phylogenomics Lee, Michael D. Bioinformatics, Vol. 35, Issue 20 https://doi.org/10.1093/bioinformatics/btz188	journal	March 2019
Extreme 13C depletion of carbonates formed during oxidation of biogenic methane in fractured granite Drake, Henrik; Åström, Mats E.; Heim, Christine Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8020	journal	May 2015
Succession in the petroleum reservoir microbiome through an oil field production lifecycle Vigneron, Adrien; Alsop, Eric B.; Lomans, Bartholomeus P. The ISME Journal, Vol. 11, Issue 9 https://doi.org/10.1038/ismej.2017.78	journal	May 2017
Bacteriophage endolysin Lyt μ1/6: characterization of the C-terminal binding domain Tišáková, Lenka; Vidová, Barbora; Farkašovská, Jarmila FEMS Microbiology Letters, Vol. 350, Issue 2 https://doi.org/10.1111/1574-6968.12338	journal	December 2013
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang Bioinformatics, Vol. 31, Issue 10 https://doi.org/10.1093/bioinformatics/btv033	journal	January 2015
How Bacteria Use Type IV Pili Machinery on Surfaces Maier, Berenike; Wong, Gerard C. L. Trends in Microbiology, Vol. 23, Issue 12 https://doi.org/10.1016/j.tim.2015.09.002	journal	December 2015
Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab301	journal	April 2021
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
Hydrogenase of the hyperthermophile Pyrococcus furiosus is an elemental sulfur reductase or sulfhydrogenase: evidence for a sulfur-reducing hydrogenase ancestor. Ma, K.; Schicho, R. N.; Kelly, R. M. Proceedings of the National Academy of Sciences, Vol. 90, Issue 11 https://doi.org/10.1073/pnas.90.11.5341	journal	June 1993
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Single cell activity reveals direct electron transfer in methanotrophic consortia McGlynn, Shawn E.; Chadwick, Grayson L.; Kempes, Christopher P. Nature, Vol. 526, Issue 7574 https://doi.org/10.1038/nature15512	journal	September 2015
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Metatranscriptomes Reveal That All Three Domains of Life Are Active but Are Dominated by Bacteria in the Fennoscandian Crystalline Granitic Continental Deep Biosphere Lopez-Fernandez, Margarita; Simone, Domenico; Wu, Xiaofen mBio, Vol. 9, Issue 6 https://doi.org/10.1128/mBio.01792-18	journal	November 2018
Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling Castelle, Cindy J.; Wrighton, Kelly C.; Thomas, Brian C. Current Biology, Vol. 25, Issue 6 https://doi.org/10.1016/j.cub.2015.01.014	journal	March 2015
Microbial communities and their predicted metabolic characteristics in deep fracture groundwaters of the crystalline bedrock at Olkiluoto, Finland Bomberg, Malin; Lamminmäki, Tiina; Itävaara, Merja Biogeosciences, Vol. 13, Issue 21 https://doi.org/10.5194/bg-13-6031-2016	journal	January 2016
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
HydDB: A web tool for hydrogenase classification and analysis Søndergaard, Dan; Pedersen, Christian N. S.; Greening, Chris Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34212	journal	September 2016
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database Chaumeil, Pierre-Alain; Mussig, Aaron J.; Hugenholtz, Philip Bioinformatics https://doi.org/10.1093/bioinformatics/btz848	journal	November 2019
Anaerobic Methanotrophic Archaea of the ANME-2d Cluster Are Active in a Low-sulfate, Iron-rich Freshwater Sediment Weber, Hannah S.; Habicht, Kirsten S.; Thamdrup, Bo Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00619	journal	April 2017
Binning metagenomic contigs by coverage and composition Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino Nature Methods, Vol. 11, Issue 11 https://doi.org/10.1038/nmeth.3103	journal	September 2014
Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer Wrighton, Kelly C.; Castelle, Cindy J.; Wilkins, Michael J. The ISME Journal, Vol. 8, Issue 7 https://doi.org/10.1038/ismej.2013.249	journal	March 2014
IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering Ma, Ze-Qiang; Dasari, Surendra; Chambers, Matthew C. Journal of Proteome Research, Vol. 8, Issue 8 https://doi.org/10.1021/pr900360j	journal	August 2009
Biogenic methane production from coal: A review on recent research and development on microbially enhanced coalbed methane (MECBM) Park, Stephen Y.; Liang, Yanna Fuel, Vol. 166 https://doi.org/10.1016/j.fuel.2015.10.121	journal	February 2016
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen Krogh, Anders; Larsson, Björn; von Heijne, Gunnar Journal of Molecular Biology, Vol. 305, Issue 3 https://doi.org/10.1006/jmbi.2000.4315	journal	January 2001
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon The ISME Journal, Vol. 11, Issue 12 https://doi.org/10.1038/ismej.2017.126	journal	July 2017
Critical biogeochemical functions in the subsurface are associated with bacteria from new phyla and little studied lineages: N- and C-cycling organisms in the subsurface Hug, Laura A.; Thomas, Brian C.; Sharon, Itai Environmental Microbiology, Vol. 18, Issue 1 https://doi.org/10.1111/1462-2920.12930	journal	July 2015
CDD/SPARCLE: the conserved domain database in 2020 Lu, Shennan; Wang, Jiyao; Chitsaz, Farideh Nucleic Acids Research, Vol. 48, Issue D1 https://doi.org/10.1093/nar/gkz991	journal	November 2019
Members of the Candidate Phyla Radiation are functionally differentiated by carbon- and nitrogen-cycling capabilities Danczak, R. E.; Johnston, M. D.; Kenah, C. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0331-1	journal	September 2017
Methyl-compound use and slow growth characterize microbial life in 2-km-deep subseafloor coal and shale beds Trembath-Reichert, Elizabeth; Morono, Yuki; Ijiri, Akira Proceedings of the National Academy of Sciences, Vol. 114, Issue 44 https://doi.org/10.1073/pnas.1707525114	journal	October 2017
Zero-valent sulphur is a key intermediate in marine methane oxidation Milucka, Jana; Ferdelman, Timothy G.; Polerecky, Lubos Nature, Vol. 491, Issue 7425 https://doi.org/10.1038/nature11656	journal	November 2012
KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold Aramaki, Takuya; Blanc-Mathieu, Romain; Endo, Hisashi Bioinformatics, Vol. 36, Issue 7 https://doi.org/10.1093/bioinformatics/btz859	journal	November 2019
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
FastUniq: A Fast De Novo Duplicates Removal Tool for Paired Short Reads Xu, Haibin; Luo, Xiang; Qian, Jun PLoS ONE, Vol. 7, Issue 12 https://doi.org/10.1371/journal.pone.0052249	journal	December 2012
Pfam: the protein families database Finn, Robert D.; Bateman, Alex; Clements, Jody Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1223	journal	November 2013
PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes Yu, Nancy Y.; Wagner, James R.; Laird, Matthew R. Bioinformatics, Vol. 26, Issue 13 https://doi.org/10.1093/bioinformatics/btq249	journal	May 2010
MyriMatch: Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C. Journal of Proteome Research, Vol. 6, Issue 2 https://doi.org/10.1021/pr0604054	journal	February 2007
Deep subseafloor microbial cells on physiological standby Jorgensen, B. B. Proceedings of the National Academy of Sciences, Vol. 108, Issue 45 https://doi.org/10.1073/pnas.1115421108	journal	October 2011
Microbial life under extreme energy limitation Hoehler, Tori M.; Jørgensen, Bo Barker Nature Reviews Microbiology, Vol. 11, Issue 2 https://doi.org/10.1038/nrmicro2939	journal	January 2013
Energy efficiency and biological interactions define the core microbiome of deep oligotrophic groundwater Mehrshad, Maliheh; Lopez-Fernandez, Margarita; Sundh, John Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-24549-z	journal	July 2021
Characterization of the locus encoding the [Ni-Fe] sulfhydrogenase from the archaeon Pyrococcus furiosus: evidence for a relationship to bacterial sulfite reductases Pedroni, P.; Volpe, A. D.; Galli, G. Microbiology, Vol. 141, Issue 2 https://doi.org/10.1099/13500872-141-2-449	journal	February 1995
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
ANME ‐1 archaea may drive methane accumulation and removal in estuarine sediments Kevorkian, Richard T.; Callahan, Sean; Winstead, Rachel Environmental Microbiology Reports, Vol. 13, Issue 2 https://doi.org/10.1111/1758-2229.12926	journal	January 2021
Microbial turnover times in the deep seabed studied by amino acid racemization modelling Braun, Stefan; Mhatre, Snehit S.; Jaussi, Marion Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-05972-z	journal	July 2017
Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae Leu, Andy O.; Cai, Chen; McIlroy, Simon J. The ISME Journal, Vol. 14, Issue 4 https://doi.org/10.1038/s41396-020-0590-x	journal	January 2020
Diversity of Sulfur-Disproportionating Microorganisms Slobodkin, A. I.; Slobodkina, G. B. Microbiology, Vol. 88, Issue 5 https://doi.org/10.1134/S0026261719050138	journal	September 2019
The origin, source, and cycling of methane in deep crystalline rock biosphere Kietäväinen, Riikka Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00725	journal	January 2015
Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales Daly, Rebecca A.; Borton, Mikayla A.; Wilkins, Michael J. Nature Microbiology, Vol. 1, Issue 10 https://doi.org/10.1038/nmicrobiol.2016.146	journal	September 2016
Manganese/iron‐supported sulfate‐dependent anaerobic oxidation of methane by archaea in lake sediments Su, Guangyi; Zopfi, Jakob; Yao, Haoyi Limnology and Oceanography, Vol. 65, Issue 4 https://doi.org/10.1002/lno.11354	journal	November 2019
Rapid Reactivation of Deep Subsurface Microbes in the Presence of C-1 Compounds Rajala, Pauliina; Bomberg, Malin; Kietäväinen, Riikka Microorganisms, Vol. 3, Issue 1 https://doi.org/10.3390/microorganisms3010017	journal	February 2015
Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments Hernsdorf, Alex W.; Amano, Yuki; Miyakawa, Kazuya The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.39	journal	March 2017
Archaea catalyze iron-dependent anaerobic oxidation of methane Ettwig, Katharina F.; Zhu, Baoli; Speth, Daan Proceedings of the National Academy of Sciences, Vol. 113, Issue 45 https://doi.org/10.1073/pnas.1609534113	journal	October 2016
Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium Desulfurivibrio alkaliphilus by Sulfide Oxidation with Nitrate Thorup, Casper; Schramm, Andreas; Findlay, Alyssa J. mBio, Vol. 8, Issue 4 https://doi.org/10.1128/mBio.00671-17	journal	July 2017
Note: Desulfovibrio aespoeensis sp. nov., a mesophilic sulfate-reducing bacterium from deep groundwater at aspo hard rock laboratory, Sweden Motamedi, M.; Pedersen, K. International Journal of Systematic Bacteriology, Vol. 48, Issue 1 https://doi.org/10.1099/00207713-48-1-311	journal	January 1998
Ecological and genomic profiling of anaerobic methane-oxidizing archaea in a deep granitic environment Ino, Kohei; Hernsdorf, Alex W.; Konno, Uta The ISME Journal, Vol. 12, Issue 1 https://doi.org/10.1038/ismej.2017.140	journal	September 2017
The biomass and biodiversity of the continental subsurface Magnabosco, C.; Lin, L. -H.; Dong, H. Nature Geoscience, Vol. 11, Issue 10 https://doi.org/10.1038/s41561-018-0221-6	journal	September 2018
Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes Butler, Jessica E.; Young, Nelson D.; Lovley, Derek R. BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-40	journal	January 2010
Deep microbial life in high-quality granitic groundwater from geochemically and geographically distinct underground boreholes: Deep microbial life in granitic aquifers Ino, Kohei; Konno, Uta; Kouduka, Mariko Environmental Microbiology Reports, Vol. 8, Issue 2 https://doi.org/10.1111/1758-2229.12379	journal	January 2016
Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations Castelle, Cindy J.; Brown, Christopher T.; Anantharaman, Karthik Nature Reviews Microbiology, Vol. 16, Issue 10 https://doi.org/10.1038/s41579-018-0076-2	journal	September 2018
Anthropogenic and Environmental Constraints on the Microbial Methane Cycle in Coastal Sediments Wallenius, Anna J.; Dalcin Martins, Paula; Slomp, Caroline P. Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.631621	journal	February 2021
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Large Scale Mapping of Fractures and Groundwater Pathways in Crystalline Hardrock By AEM Chandra, Subash; Auken, Esben; Maurya, Pradip K. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-36153-1	journal	January 2019
Anaerobic Oxidation of Methane: Progress with an Unknown Process Knittel, Katrin; Boetius, Antje Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.61.080706.093130	journal	October 2009
Genome‐inferred spatio‐temporal resolution of an uncultivated Roizmanbacterium reveals its ecological preferences in groundwater Geesink, Patricia; Wegner, Carl‐Eric; Probst, Alexander J. Environmental Microbiology, Vol. 22, Issue 2 https://doi.org/10.1111/1462-2920.14865	journal	December 2019
Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy Sieber, Christian M. K.; Probst, Alexander J.; Sharrar, Allison Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0171-1	journal	May 2018
Biogenic processes in crystalline bedrock fractures indicated by carbon isotope signatures of secondary calcite Sahlstedt, Elina; Karhu, Juha A.; Pitkänen, Petteri Applied Geochemistry, Vol. 67 https://doi.org/10.1016/j.apgeochem.2016.01.010	journal	April 2016
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Biogeochemical Cycling by a Low-Diversity Microbial Community in Deep Groundwater Bell, Emma; Lamminmäki, Tiina; Alneberg, Johannes Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02129	journal	September 2018
Environmental proteomics reveals early microbial community responses to biostimulation at a uranium- and nitrate-contaminated site Chourey, Karuna; Nissen, Silke; Vishnivetskaya, Tatiana PROTEOMICS https://doi.org/10.1002/pmic.201300155	journal	August 2013
Reconstructing a hydrogen-driven microbial metabolic network in Opalinus Clay rock Bagnoud, Alexandre; Chourey, Karuna; Hettich, Robert L. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12770	journal	October 2016
A methanotrophic archaeon couples anaerobic oxidation of methane to Fe(III) reduction Cai, Chen; Leu, Andy O.; Xie, Guo-Jun The ISME Journal, Vol. 12, Issue 8 https://doi.org/10.1038/s41396-018-0109-x	journal	April 2018
Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage Haroon, Mohamed F.; Hu, Shihu; Shi, Ying Nature, Vol. 500, Issue 7464 https://doi.org/10.1038/nature12375	journal	July 2013
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle He, Xuesong; McLean, Jeffrey S.; Edlund, Anna Proceedings of the National Academy of Sciences, Vol. 112, Issue 1 https://doi.org/10.1073/pnas.1419038112	journal	December 2014
Enzyme phylogenies as markers for the oxidation state of the environment: The case of respiratory arsenate reductase and related enzymes Duval, Simon; Ducluzeau, Anne-Lise; Nitschke, Wolfgang BMC Evolutionary Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2148-8-206	journal	January 2008
Gene expression and ultrastructure of meso- and thermophilic methanotrophic consortia: Interspecies interaction within AOM consortia Krukenberg, Viola; Riedel, Dietmar; Gruber-Vodicka, Harald R. Environmental Microbiology, Vol. 20, Issue 5 https://doi.org/10.1111/1462-2920.14077	journal	April 2018
Understanding and modelling dissolved gas transport in the bedrock of three Fennoscandian sites Trinchero, Paolo; Delos, Anne; Molinero, Jorge Journal of Hydrology, Vol. 512 https://doi.org/10.1016/j.jhydrol.2014.03.011	journal	May 2014
Global diffusive fluxes of methane in marine sediments Egger, Matthias; Riedinger, Natascha; Mogollón, José M. Nature Geoscience, Vol. 11, Issue 6 https://doi.org/10.1038/s41561-018-0122-8	journal	May 2018
Severe Corrosion of Carbon Steel in Oil Field Produced Water Can Be Linked to Methanogenic Archaea Containing a Special Type of [NiFe] Hydrogenase Lahme, Sven; Mand, Jaspreet; Longwell, John Applied and Environmental Microbiology, Vol. 87, Issue 3 https://doi.org/10.1128/AEM.01819-20	journal	January 2021
High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries Jain, Chirag; Rodriguez-R, Luis M.; Phillippy, Adam M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07641-9	journal	November 2018
Diverse uncultivated ultra-small bacterial cells in groundwater Luef, Birgit; Frischkorn, Kyle R.; Wrighton, Kelly C. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7372	journal	February 2015
Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle Anantharaman, Karthik; Hausmann, Bela; Jungbluth, Sean P. The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0078-0	journal	February 2018
An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers Lau, Maggie C. Y.; Kieft, Thomas L.; Kuloyo, Olukayode Proceedings of the National Academy of Sciences, Vol. 113, Issue 49 https://doi.org/10.1073/pnas.1612244113	journal	November 2016
Biological souring and mitigation in oil reservoirs Gieg, Lisa M.; Jack, Tom R.; Foght, Julia M. Applied Microbiology and Biotechnology, Vol. 92, Issue 2 https://doi.org/10.1007/s00253-011-3542-6	journal	August 2011
Metabolic activity of subterranean microbial communities in deep granitic groundwater supplemented with methane and H2 Pedersen, Karsten The ISME Journal, Vol. 7, Issue 4 https://doi.org/10.1038/ismej.2012.144	journal	December 2012
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies Kang, Dongwan D.; Li, Feng; Kirton, Edward PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7359	journal	January 2019
Anaerobic oxidation of ethane by archaea from a marine hydrocarbon seep Chen, Song-Can; Musat, Niculina; Lechtenfeld, Oliver J. Nature, Vol. 568, Issue 7750 https://doi.org/10.1038/s41586-019-1063-0	journal	March 2019
Near-optimal probabilistic RNA-seq quantification Bray, Nicolas L.; Pimentel, Harold; Melsted, Páll Nature Biotechnology, Vol. 34, Issue 5 https://doi.org/10.1038/nbt.3519	journal	April 2016
RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria Wrighton, Kelly C.; Castelle, Cindy J.; Varaljay, Vanessa A. The ISME Journal, Vol. 10, Issue 11 https://doi.org/10.1038/ismej.2016.53	journal	May 2016
Microbiological disproportionation of inorganic sulfur compounds Finster, Kai Journal of Sulfur Chemistry, Vol. 29, Issue 3-4 https://doi.org/10.1080/17415990802105770	journal	August 2008

Similar Records

Ecological and genomic profiling of anaerobic methane-oxidizing archaea in a deep granitic environment

Journal Article · Fri Sep 08 00:00:00 EDT 2017 · The ISME Journal · OSTI ID:1845369

Ino, Kohei; Hernsdorf, Alex W.; Konno, Uta; +17 more

Active sulfur cycling in the terrestrial deep subsurface

Journal Article · Tue Feb 11 00:00:00 EST 2020 · The ISME Journal · OSTI ID:1845369

Bell, Emma; Lamminmäki, Tiina; Alneberg, Johannes; +6 more

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

Journal Article · Fri Sep 07 00:00:00 EDT 2018 · Frontiers in Microbiology · OSTI ID:1845369

Bell, Emma; Lamminmäki, Tiina; Alneberg, Johannes; +8 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Active anaerobic methane oxidation and sulfur disproportionation in the deep terrestrial subsurface

Citation Formats

References (102)

Similar Records

Related Subjects