Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO2 concentrations

Probst, Alexander J.; Castelle, Cindy J.; Singh, Andrea; Brown, Christopher T.; Anantharaman, Karthik; Sharon, Itai; Hug, Laura A.; Burstein, David; Emerson, Joanne B.; Thomas, Brian C.; Banfield, Jillian F.

doi:10.1111/1462-2920.13362

Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO₂ concentrations

Journal Article · Tue Apr 26 04:00:00 EDT 2016 · Environmental Microbiology

DOI:https://doi.org/10.1111/1462-2920.13362· OSTI ID:1567074

Probst, Alexander J. ^[1]; Castelle, Cindy J. ^[1]; Singh, Andrea ^[1]; Brown, Christopher T. ^[1]; Anantharaman, Karthik ^[1]; Sharon, Itai ^[1]; Hug, Laura A. ^[1]; Burstein, David ^[1]; Emerson, Joanne B. ^[1]; Thomas, Brian C. ^[1]; Banfield, Jillian F. ^[2]

Univ. of California, Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

As in many deep underground environments, the microbial communities in subsurface high-CO₂ ecosystems remain relatively unexplored. Current research based on single-gene assays revealed a remarkable variety of organisms from little studied phyla in Crystal Geyser (Utah, USA), a site where deeply sourced CO₂-saturated fluids are erupted at the surface. To provide genomic resolution of the metabolisms of these organisms, we used a novel metagenomic approach to recover 227 high-quality genomes from 150 microbial species affiliated with 46 different phylum-level lineages. Bacteria from two novel phylum-level lineages have the capacity for CO₂ fixation. Analyses of carbon fixation pathways in all studied organisms revealed that the Wood-Ljungdahl pathway and the Calvin-Benson-Bassham Cycle occurred with the highest frequency, whereas the reverse TCA cycle was little used. We infer that this, and selection for form II RuBisCOs, are adaptions to high CO₂-concentrations. Yet, many autotrophs can also grow mixotrophically, a strategy that confers metabolic versatility. The assignment of 156 hydrogenases to 90 different organisms suggests that H₂ is an important inter-species energy currency even under gaseous CO₂-saturation. As a whole, metabolic analyses at the organism level provided insight into the biochemical cycles that support subsurface life under the extreme condition of CO₂ saturation.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1567074

Journal Information:: Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 2 Vol. 19; ISSN 1462-2912

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

Natural and industrial analogues for leakage of CO2 from storage reservoirs: identification of features, events, and processes and lessons learned Lewicki, Jennifer L.; Birkholzer, Jens; Tsang, Chin-Fu Environmental Geology, Vol. 52, Issue 3 https://doi.org/10.1007/s00254-006-0479-7	journal	October 2006
A missing link between complex I and group 4 membrane-bound [NiFe] hydrogenases Marreiros, Bruno C.; Batista, Ana P.; Duarte, Afonso M. S. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2 https://doi.org/10.1016/j.bbabio.2012.09.012	journal	February 2013
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
Monitoring petrophysical, mineralogical, geochemical and microbiological effects of CO2 exposure — Results of long-term experiments under in situ conditions Wandrey, Maren; Fischer, Sebastian; Zemke, Kornelia Energy Procedia, Vol. 4 https://doi.org/10.1016/j.egypro.2011.02.295	journal	January 2011
Microbial community and inorganic fluid analysis during CO2 storage within the frame of CO2SINK–Long-term experiments under in situ conditions Wandrey, Maren; Pellizari, Linda; Zettlitzer, Michael Energy Procedia, Vol. 4 https://doi.org/10.1016/j.egypro.2011.02.296	journal	January 2011
Eruption dynamics of CO2-driven cold-water geysers: Crystal, Tenmile geysers in Utah and Chimayó geyser in New Mexico Watson, Z. T.; Han, Weon Shik; Keating, Elizabeth H. Earth and Planetary Science Letters, Vol. 408 https://doi.org/10.1016/j.epsl.2014.10.001	journal	December 2014
The range and level of impurities in CO2 streams from different carbon capture sources Porter, Richard T. J.; Fairweather, Michael; Pourkashanian, Mohamed International Journal of Greenhouse Gas Control, Vol. 36 https://doi.org/10.1016/j.ijggc.2015.02.016	journal	May 2015
“Candidatus Sonnebornia yantaiensis”, a member of candidate division OD1, as intracellular bacteria of the ciliated protist Paramecium bursaria (Ciliophora, Oligohymenophorea) Gong, Jun; Qing, Yao; Guo, Xiaohong Systematic and Applied Microbiology, Vol. 37, Issue 1 https://doi.org/10.1016/j.syapm.2013.08.007	journal	February 2014
Regulating the Ultimate Sink: Managing the Risks of Geologic CO₂ Storage Wilson, Elizabeth J.; Johnson, Timothy L.; Keith, David W. Environmental Science & Technology, Vol. 37, Issue 16 https://doi.org/10.1021/es021038+	journal	July 2003
Hydrogeochemical characterization of leaking, carbon dioxide-charged fault zones in east-central Utah, with implications for geologic carbon storage Heath, Jason E.; Lachmar, Thomas E.; Evans, James P. Carbon Sequestration and Its Role in the Global Carbon Cycle https://doi.org/10.1029/2006GM000407	book	January 2009
Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community Handley, Kim M.; VerBerkmoes, Nathan C.; Steefel, Carl I. The ISME Journal, Vol. 7, Issue 4 https://doi.org/10.1038/ismej.2012.148	journal	November 2012
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
Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival Greening, Chris; Biswas, Ambarish; Carere, Carlo R. The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.153	journal	September 2015
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
Unusual biology across a group comprising more than 15% of domain Bacteria Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C. Nature, Vol. 523, Issue 7559 https://doi.org/10.1038/nature14486	journal	June 2015
Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment Castelle, Cindy J.; Hug, Laura A.; Wrighton, Kelly C. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3120	journal	August 2013
Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface Probst, Alexander J.; Weinmaier, Thomas; Raymann, Kasie Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6497	journal	November 2014
Geological carbon storage Bickle, Mike J. Nature Geoscience, Vol. 2, Issue 12 https://doi.org/10.1038/ngeo687	journal	December 2009
Autotrophic carbon fixation in archaea Berg, Ivan A.; Kockelkorn, Daniel; Ramos-Vera, W. Hugo Nature Reviews Microbiology, Vol. 8, Issue 6, p. 447-460 https://doi.org/10.1038/nrmicro2365	journal	May 2010
Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences Yarza, Pablo; Yilmaz, Pelin; Pruesse, Elmar Nature Reviews Microbiology, Vol. 12, Issue 9 https://doi.org/10.1038/nrmicro3330	journal	August 2014
ATP-citrate lyase from the green sulfur bacterium Chlorobium limicola is a heteromeric enzyme composed of two distinct gene products : ATP-citrate lyase from Kanao, Tadayoshi; Fukui, Toshiaki; Atomi, Haruyuki European Journal of Biochemistry, Vol. 268, Issue 6 https://doi.org/10.1046/j.1432-1327.2001.02034.x	journal	March 2001
Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation Konneke, M.; Schubert, D. M.; Brown, P. C. Proceedings of the National Academy of Sciences, Vol. 111, Issue 22 https://doi.org/10.1073/pnas.1402028111	journal	May 2014
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
Prokaryotes: The unseen majority Whitman, W. B.; Coleman, D. C.; Wiebe, W. J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 12 https://doi.org/10.1073/pnas.95.12.6578	journal	June 1998
Separation and Capture of CO ₂ from Large Stationary Sources and Sequestration in Geological Formations—Coalbeds and Deep Saline Aquifers White, Curt M.; Strazisar, Brian R.; Granite, Evan J. Journal of the Air & Waste Management Association, Vol. 53, Issue 6 https://doi.org/10.1080/10473289.2003.10466206	journal	June 2003
RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees Stamatakis, A.; Ludwig, T.; Meier, H. Bioinformatics, Vol. 21, Issue 4 https://doi.org/10.1093/bioinformatics/bti191	journal	December 2004
UniRef: comprehensive and non-redundant UniProt reference clusters Suzek, B. E.; Huang, H.; McGarvey, P. Bioinformatics, Vol. 23, Issue 10 https://doi.org/10.1093/bioinformatics/btm098	journal	March 2007
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
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle Badger, Murray Ronald; Bek, Emily Jane Journal of Experimental Botany, Vol. 59, Issue 7 https://doi.org/10.1093/jxb/erm297	journal	February 2008
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
Fast algorithms for large-scale genome alignment and comparison Delcher, A. L. Nucleic Acids Research, Vol. 30, Issue 11 https://doi.org/10.1093/nar/30.11.2478	journal	June 2002
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
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB Pruesse, E.; Quast, C.; Knittel, K. Nucleic Acids Research, Vol. 35, Issue 21 https://doi.org/10.1093/nar/gkm864	journal	November 2007
Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group Nunoura, Takuro; Takaki, Yoshihiro; Kakuta, Jungo Nucleic Acids Research, Vol. 39, Issue 8 https://doi.org/10.1093/nar/gkq1228	journal	December 2010
HMMER web server: interactive sequence similarity searching Finn, R. D.; Clements, J.; Eddy, S. R. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr367	journal	May 2011
MicroScope—an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data Vallenet, David; Belda, Eugeni; Calteau, Alexandra Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1194	journal	November 2012
Rfam 12.0: updates to the RNA families database Nawrocki, Eric P.; Burge, Sarah W.; Bateman, Alex Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1063	journal	November 2014
Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization Sharon, I.; Morowitz, M. J.; Thomas, B. C. Genome Research, Vol. 23, Issue 1 https://doi.org/10.1101/gr.142315.112	journal	August 2012
Metagenomic analysis of a high carbon dioxide subsurface microbial community populated by chemolithoautotrophs and bacteria and archaea from candidate phyla: High CO Emerson, Joanne B.; Thomas, Brian C.; Alvarez, Walter Environmental Microbiology, Vol. 18, Issue 6 https://doi.org/10.1111/1462-2920.12817	journal	April 2015
Single-cell genomics of uncultivated deep-branching magnetotactic bacteria reveals a conserved set of magnetosome genes: Genomic analysis of an uncultivated multicellular magnetotactic prokaryote Kolinko, Sebastian; Richter, Michael; Glöckner, Frank-Oliver Environmental Microbiology, Vol. 18, Issue 1 https://doi.org/10.1111/1462-2920.12907	journal	July 2015
Characteristics of CO ₂ -driven cold-water geyser, Crystal Geyser in Utah: experimental observation and mechanism analyses Han, W. S.; Lu, M.; McPherson, B. J. Geofluids, Vol. 13, Issue 3 https://doi.org/10.1111/gfl.12018	journal	February 2013
Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes Eiler, Alexander; Bertilsson, Stefan Environmental Microbiology, Vol. 6, Issue 12 https://doi.org/10.1111/j.1462-2920.2004.00657.x	journal	December 2004
Phylogenetic diversity and metagenomics of candidate division OP3: Candidate division OP3 Glöckner, Jana; Kube, Michael; Shrestha, Pravin Malla Environmental Microbiology, Vol. 12, Issue 5 https://doi.org/10.1111/j.1462-2920.2010.02164.x	journal	February 2010
Single-cell analysis reveals a novel uncultivated magnetotactic bacterium within the candidate division OP3: Uncultivated MTB in candidate division OP3 Kolinko, Sebastian; Jogler, Christian; Katzmann, Emanuel Environmental Microbiology, Vol. 14, Issue 7 https://doi.org/10.1111/j.1462-2920.2011.02609.x	journal	October 2011
Comparison of prokaryotic diversity at offshore oceanic locations reveals a different microbiota in the Mediterranean Sea: Offshore prokaryotic diversity Zaballos, Milagros; LÃ³pez-LÃ³pez, Arantxa; Ovreas, Lise FEMS Microbiology Ecology, Vol. 56, Issue 3 https://doi.org/10.1111/j.1574-6941.2006.00060.x	journal	June 2006
Lineages of Acidophilic Archaea Revealed by Community Genomic Analysis Baker, Brett J.; Tyson, Gene W.; Webb, Richard I. Science, Vol. 314, Issue 5807 https://doi.org/10.1126/science.1132690	journal	December 2006
Physiological Proteomics of the Uncultured Endosymbiont of Riftia pachyptila Markert, S.; Arndt, C.; Felbeck, H. Science, Vol. 315, Issue 5809 https://doi.org/10.1126/science.1132913	journal	January 2007
Archaeal Type III RuBisCOs Function in a Pathway for AMP Metabolism Sato, T.; Atomi, H.; Imanaka, T. Science, Vol. 315, Issue 5814 https://doi.org/10.1126/science.1135999	journal	February 2007
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
Axenic Culture of a Candidate Division TM7 Bacterium from the Human Oral Cavity and Biofilm Interactions with Other Oral Bacteria Soro, Valeria; Dutton, Lindsay C.; Sprague, Susan V. Applied and Environmental Microbiology, Vol. 80, Issue 20 https://doi.org/10.1128/AEM.01827-14	journal	August 2014
Ecological Aspects of the Distribution of Different Autotrophic CO ₂ Fixation Pathways Berg, Ivan A. Applied and Environmental Microbiology, Vol. 77, Issue 6 https://doi.org/10.1128/AEM.02473-10	journal	January 2011
Large Fractions of CO ₂ -Fixing Microorganisms in Pristine Limestone Aquifers Appear To Be Involved in the Oxidation of Reduced Sulfur and Nitrogen Compounds Herrmann, Martina; Rusznyák, Anna; Akob, Denise M. Applied and Environmental Microbiology, Vol. 81, Issue 7 https://doi.org/10.1128/AEM.03269-14	journal	January 2015
The Iron-Hydrogenase of Thermotoga maritima Utilizes Ferredoxin and NADH Synergistically: a New Perspective on Anaerobic Hydrogen Production Schut, G. J.; Adams, M. W. W. Journal of Bacteriology, Vol. 191, Issue 13 https://doi.org/10.1128/JB.01582-08	journal	May 2009
Novel Division Level Bacterial Diversity in a Yellowstone Hot Spring Hugenholtz, Philip; Pitulle, Christian; Hershberger, Karen L. Journal of Bacteriology, Vol. 180, Issue 2 https://doi.org/10.1128/JB.180.2.366-376.1998	journal	January 1998
Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla Kantor, Rose S.; Wrighton, Kelly C.; Handley, Kim M. mBio, Vol. 4, Issue 5 https://doi.org/10.1128/mBio.00708-13	journal	October 2013
Genome-Resolved Metagenomic Analysis Reveals Roles for Candidate Phyla and Other Microbial Community Members in Biogeochemical Transformations in Oil Reservoirs Hu, Ping; Tom, Lauren; Singh, Andrea mBio, Vol. 7, Issue 1 https://doi.org/10.1128/mBio.01669-15	journal	January 2016
Genomic Insights into Syntrophy: The Paradigm for Anaerobic Metabolic Cooperation Sieber, Jessica R.; McInerney, Michael J.; Gunsalus, Robert P. Annual Review of Microbiology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-micro-090110-102844	journal	October 2012
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
Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling Hug, Laura A.; Castelle, Cindy J.; Wrighton, Kelly C. Microbiome, Vol. 1, Issue 1 https://doi.org/10.1186/2049-2618-1-22	journal	January 2013
Genetic Evidence for Bacterial Chemolithoautotrophy Based on the Reductive Tricarboxylic Acid Cycle in Groundwater Systems Alfreider, Albin; Vogt, Carsten Microbes and Environments, Vol. 27, Issue 2 https://doi.org/10.1264/jsme2.ME11274	journal	January 2012
Mariprofundus ferrooxydans PV-1 the First Genome of a Marine Fe(II) Oxidizing Zetaproteobacterium Singer, Esther; Emerson, David; Webb, Eric A. PLoS ONE, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pone.0025386	journal	September 2011
Geological Carbon Dioxide Sequestration Friedmann, S. J. Elements, Vol. 3, Issue 3 https://doi.org/10.2113/gselements.3.3.179	journal	June 2007
Timing and prediction of CO₂ eruptions from Crystal Geyser, UT Gouveia, F. J.; Friedmann, S. J. https://doi.org/10.2172/897988	report	May 2006
Changes in the deep subsurface microbial biosphere resulting from a field-scale CO2 geosequestration experiment Mu, Andre; Boreham, Chris; Leong, Henrietta X. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00209	journal	May 2014
Geology of Crystal Geyser and environmental implications of its effluent, Grand County, Utah Baer, James L.; Rigby, J. Keith Utah Geology, Vol. 5, Issue 2 https://doi.org/10.34191/UG-5-2-125	journal	January 1978
Analysis of five complete genome sequences for members of the class Peribacteria in the recently recognized Peregrinibacteria bacterial phylum Anantharaman, Karthik; Brown, Christopher T.; Burstein, David PeerJ, Vol. 4 https://doi.org/10.7717/peerj.1607	journal	January 2016

Cited By (54)

New CRISPR–Cas systems from uncultivated microbes Burstein, David; Harrington, Lucas B.; Strutt, Steven C. Nature, Vol. 542, Issue 7640 https://doi.org/10.1038/nature21059	journal	December 2016
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
The distinction of CPR bacteria from other bacteria based on protein family content Méheust, Raphaël; Burstein, David; Castelle, Cindy J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12171-z	journal	September 2019
Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface Probst, Alexander J.; Ladd, Bethany; Jarett, Jessica K. Nature Microbiology, Vol. 3, Issue 3 https://doi.org/10.1038/s41564-017-0098-y	journal	January 2018
Rice Paddy Nitrospirae Carry and Express Genes Related to Sulfate Respiration: Proposal of the New Genus “ Candidatus Sulfobium” Zecchin, Sarah; Mueller, Ralf C.; Seifert, Jana Applied and Environmental Microbiology, Vol. 84, Issue 5 https://doi.org/10.1128/aem.02224-17	journal	December 2017
RNA-Dependent Cysteine Biosynthesis in Bacteria and Archaea Mukai, Takahito; Crnković, Ana; Umehara, Takuya mBio, Vol. 8, Issue 3, Article No. e00561-17 https://doi.org/10.1128/mbio.00561-17	journal	May 2017
Validating the Cyc2 Neutrophilic Iron Oxidation Pathway Using Meta-omics of Zetaproteobacteria Iron Mats at Marine Hydrothermal Vents McAllister, Sean M.; Polson, Shawn W.; Butterfield, David A. mSystems, Vol. 5, Issue 1 https://doi.org/10.1128/msystems.00553-19	journal	February 2020
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
Capability for arsenic mobilization in groundwater is distributed across broad phylogenetic lineages Danczak, Robert E.; Johnston, Michael D.; Kenah, Chris PLOS ONE, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pone.0221694	journal	September 2019
Exemplar Abstract for Wirthibacter wanneri Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/ex.38278	dataset	January 2020
Nomenclature Abstract for Wirthibacter wanneri Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/nm.38278	dataset	January 2020
Nomenclature Abstract for Wirthbacteria Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/nm.38402	dataset	January 2020
Nomenclature Abstract for Incertae sedis 620 Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/nm.38403	dataset	January 2020
Nomenclature Abstract for Incertae sedis 621 Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/nm.38404	dataset	January 2020
Nomenclature Abstract for Incertae sedis 622 Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/nm.38405	dataset	January 2020
Taxon Abstract for the genus Wirthibacter Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/tx.38257	dataset	January 2020
Taxon Abstract for the species Wirthibacter wanneri Probst et al. 2017 Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/tx.38278	dataset	January 2020
Taxon Abstract for the order Incertae sedis 621 Probst et al. 2017 Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/tx.38404	dataset	January 2020
Taxon Abstract for the family Incertae sedis 622 Probst et al. 2017 Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/tx.38405	dataset	January 2020
Culture Independent Genomic Comparisons Reveal Environmental Adaptations for Altiarchaeales Bird, Jordan T.; Baker, Brett J.; Probst, Alexander J. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01221	journal	August 2016
Microbial Community Structure and the Persistence of Cyanobacterial Populations in Salt Crusts of the Hyperarid Atacama Desert from Genome-Resolved Metagenomics Finstad, Kari M.; Probst, Alexander J.; Thomas, Brian C. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01435	journal	July 2017
Genomic Characteristics of Desulfonema ishimotonii Tokyo 01T Implying Horizontal Gene Transfer Among Phylogenetically Dispersed Filamentous Gliding Bacteria Watanabe, Miho; Kojima, Hisaya; Umezawa, Kazuhiro Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00227	journal	February 2019
Genome of the candidate phylum Aminicenantes bacterium from a deep subsurface thermal aquifer revealed its fermentative saccharolytic lifestyle Kadnikov, Vitaly V.; Mardanov, Andrey V.; Beletsky, Alexey V. Extremophiles, Vol. 23, Issue 2 https://doi.org/10.1007/s00792-018-01073-5	journal	January 2019
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
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
Poorly known microbial taxa dominate the microbiome of permafrost thaw ponds Wurzbacher, Christian; Nilsson, R. Henrik; Rautio, Milla The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.54	journal	April 2017
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
Anaerobic hydrocarbon degradation in candidate phylum ‘Atribacteria’ (JS1) inferred from genomics Liu, Yi-Fan; Qi, Zhen-Zhen; Shou, Li-Bin The ISME Journal, Vol. 13, Issue 9 https://doi.org/10.1038/s41396-019-0448-2	journal	June 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
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
Simulation of Deepwater Horizon oil plume reveals substrate specialization within a complex community of hydrocarbon degraders Hu, Ping; Dubinsky, Eric A.; Probst, Alexander J. Proceedings of the National Academy of Sciences, Vol. 114, Issue 28 https://doi.org/10.1073/pnas.1703424114	journal	June 2017
A metagenomic window into the 2-km-deep terrestrial subsurface aquifer revealed multiple pathways of organic matter decomposition Kadnikov, Vitaly V.; Mardanov, Andrey V.; Beletsky, Alexey V. FEMS Microbiology Ecology, Vol. 94, Issue 10 https://doi.org/10.1093/femsec/fiy152	journal	August 2018
Microbial community composition of a hydrocarbon reservoir 40 years after a CO2 enhanced oil recovery flood Shelton, Jenna LK; Andrews, Robert S.; Akob, Denise M. FEMS Microbiology Ecology, Vol. 94, Issue 10 https://doi.org/10.1093/femsec/fiy153	journal	August 2018
The Fe(II)-oxidizing Zetaproteobacteria : historical, ecological and genomic perspectives McAllister, Sean M.; Moore, Ryan M.; Gartman, Amy FEMS Microbiology Ecology, Vol. 95, Issue 4 https://doi.org/10.1093/femsec/fiz015	journal	January 2019
A Journey across Genomes Uncovers the Origin of Ubiquinone in Cyanobacteria Degli Esposti, Mauro Genome Biology and Evolution, Vol. 9, Issue 11 https://doi.org/10.1093/gbe/evx225	journal	November 2017
Carbon Fixation by Marine Ultrasmall Prokaryotes Lannes, Romain; Olsson-Francis, Karen; Lopez, Philippe Genome Biology and Evolution, Vol. 11, Issue 4 https://doi.org/10.1093/gbe/evz050	journal	March 2019
Lateral Gene Transfer Shapes the Distribution of RuBisCO among Candidate Phyla Radiation Bacteria and DPANN Archaea Jaffe, Alexander L.; Castelle, Cindy J.; Dupont, Christopher L. Molecular Biology and Evolution, Vol. 36, Issue 3 https://doi.org/10.1093/molbev/msy234	journal	December 2018
Microbial metabolism and adaptations in Atribacteria-dominated methane hydrate sediments Glass, Jennifer B.; Ranjan, Piyush; Kretz, Cecilia B. Environmental Microbiology https://doi.org/10.1101/536078	journal	June 2021
Genome-reconstruction for eukaryotes from complex natural microbial communities West, Patrick T.; Probst, Alexander J.; Grigoriev, Igor V. Genome Research, Vol. 28, Issue 4 https://doi.org/10.1101/gr.228429.117	journal	March 2018
Microbial diversity of an Antarctic subglacial community and high‐resolution replicate sampling inform hydrological connectivity in a polar desert Campen, Richard; Kowalski, Julia; Lyons, W. Berry Environmental Microbiology, Vol. 21, Issue 7 https://doi.org/10.1111/1462-2920.14607	journal	April 2019
Microbial metabolism and adaptations in Atribacteria ‐dominated methane hydrate sediments Glass, Jennifer B.; Ranjan, Piyush; Kretz, Cecilia B. Environmental Microbiology, Vol. 23, Issue 8 https://doi.org/10.1111/1462-2920.15656	journal	July 2021
Insights into microbial community structure and function from a shallow, simulated CO ₂ ‐leakage aquifer demonstrate microbial selection and adaptation Gulliver, Djuna; Lipus, Daniel; Ross, Daniel Environmental Microbiology Reports, Vol. 11, Issue 3 https://doi.org/10.1111/1758-2229.12675	journal	August 2018
Programmed DNA destruction by miniature CRISPR-Cas14 enzymes Harrington, Lucas B.; Burstein, David; Chen, Janice S. Science, Vol. 362, Issue 6416 https://doi.org/10.1126/science.aav4294	journal	October 2018
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
Genome-resolved metagenomics analysis provides insights into the ecological role of Thaumarchaeota in the Amazon River and its plume Pinto, Otávio H. B.; Silva, Thais F.; Vizzotto, Carla S. BMC Microbiology, Vol. 20, Issue 1 https://doi.org/10.1186/s12866-020-1698-x	journal	January 2020
The rise of diversity in metabolic platforms across the Candidate Phyla Radiation Jaffe, Alexander L.; Castelle, Cindy J.; Matheus Carnevali, Paula B. BMC Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12915-020-00804-5	journal	June 2020
Insights into the ecology, evolution, and metabolism of the widespread Woesearchaeotal lineages Liu, Xiaobo; Li, Meng; Castelle, Cindy J. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0488-2	journal	June 2018
A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments Vavourakis, Charlotte D.; Andrei, Adrian-Stefan; Mehrshad, Maliheh Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0548-7	journal	September 2018
Increased replication of dissimilatory nitrate-reducing bacteria leads to decreased anammox bioreactor performance Keren, Ray; Lawrence, Jennifer E.; Zhuang, Weiqin Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-0786-3	journal	January 2020
Structure and function of archaeal histones Henneman, Bram; van Emmerik, Clara; van Ingen, Hugo PLOS Genetics, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pgen.1007582	journal	September 2018
Taxon Abstract for the Domain Archaea Woese, C. R. NamesforLife https://doi.org/10.1601/tx.1	dataset	January 1990
Taxon Abstract for the class Incertae sedis 620 Probst et al. 2017 Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/tx.38403	dataset	January 2020
New Biological Insights Into How Deforestation in Amazonia Affects Soil Microbial Communities Using Metagenomics and Metagenome-Assembled Genomes Kroeger, Marie E.; Delmont, Tom O.; Eren, A. M. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01635	journal	July 2018
Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone Butterfield, Cristina N.; Li, Zhou; Andeer, Peter F. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2687	journal	January 2016