Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment

Castelle, Cindy J.; Hug, Laura A.; Wrighton, Kelly C.; Thomas, Brian C.; Williams, Kenneth H.; Wu, Dongying; Tringe, Susannah G.; Singer, Steven W.; Eisen, Jonathan A.; Banfield, Jillian F.

doi:10.1038/ncomms3120

Title: Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment

Journal Article · Tue Aug 27 00:00:00 EDT 2013 · Nature Communications

DOI:https://doi.org/10.1038/ncomms3120· OSTI ID:1407195

Castelle, Cindy J. ^[1]; Hug, Laura A. ^[1]; Wrighton, Kelly C. ^[1]; Thomas, Brian C. ^[1]; Williams, Kenneth H. ^[2]; Wu, Dongying ^[3]; Tringe, Susannah G. ^[4]; Singer, Steven W. ^[2]; Eisen, Jonathan A. ^[5]; Banfield, Jillian F. ^[6]

Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division
Univ. of California, Davis, CA (United States). UC Davis Genome Center
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics Division
Univ. of California, Davis, CA (United States). UC Davis Genome Center. Dept. of Evolution and Ecology. Dept. of Medical Microbiology and Immunology
Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division

Microorganisms in the subsurface represent a substantial but poorly understood component of the Earth’s biosphere. Subsurface environments are complex and difficult to characterize; thus, their microbiota have remained as a ‘dark matter’ of the carbon and other biogeochemical cycles. Here we deeply sequence two sediment-hosted microbial communities from an aquifer adjacent to the Colorado River, CO, USA. No single organism represents more than ~1% of either community. Remarkably, many bacteria and archaea in these communities are novel at the phylum level or belong to phyla lacking a sequenced representative. The dominant organism in deeper sediment, RBG-1, is a member of a new phylum. On the basis of its reconstructed complete genome, RBG-1 is metabolically versatile. Its wide respiration-based repertoire may enable it to respond to the fluctuating redox environment close to the water table. We document extraordinary microbial novelty and the importance of previously unknown lineages in sediment biogeochemical transformations.

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

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

Grant/Contract Number:: AC02-05CH11231; SC0004733

OSTI ID:: 1407195

Journal Information:: Nature Communications, Vol. 4; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 145 works

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Fungi Contribute Critical but Spatially Varying Roles in Nitrogen and Carbon Cycling in Acid Mine Drainage Mosier, Annika C.; Miller, Christopher S.; Frischkorn, Kyle R. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00238	journal	March 2016
Genomic and Transcriptomic Resolution of Organic Matter Utilization Among Deep-Sea Bacteria in Guaymas Basin Hydrothermal Plumes Li, Meng; Jain, Sunit; Dick, Gregory J. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01125	journal	July 2016
Stable and Variable Parts of Microbial Community in Siberian Deep Subsurface Thermal Aquifer System Revealed in a Long-Term Monitoring Study Frank, Yulia A.; Kadnikov, Vitaly V.; Gavrilov, Sergey N. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.02101	journal	December 2016
Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer Jewell, Talia N. M.; Karaoz, Ulas; Bill, Markus Frontiers in Microbiology, Vol. 8, Article No. 40 https://doi.org/10.3389/fmicb.2017.00040	journal	January 2017
High-Throughput Sequencing Analysis of the Actinobacterial Spatial Diversity in Moonmilk Deposits Maciejewska, Marta; Całusińska, Magdalena; Cornet, Luc Antibiotics, Vol. 7, Issue 2 https://doi.org/10.3390/antibiotics7020027	journal	March 2018
Crowdsourcing the identification of organisms: A case-study of iSpot Silvertown, Jonathan; Harvey, Martin; Greenwood, Richard ZooKeys, Vol. 480 https://doi.org/10.3897/zookeys.480.8803	journal	February 2015
Spatial variations of microbial communities in abyssal and hadal sediments across the Challenger Deep Cui, Guojie; Li, Jun; Gao, Zhaoming PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6961	journal	January 2019
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
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
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
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
Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria Matheus Carnevali, Paula B.; Schulz, Frederik; Castelle, Cindy J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-018-08246-y	journal	January 2019
Influence of pH on the balance between methanogenesis and iron reduction Marquart, Kyle A.; Haller, Ben R.; Paper, Janet M. Geobiology, Vol. 17, Issue 2 https://doi.org/10.1111/gbi.12320	journal	November 2018
The response of dominant and rare taxa for fungal diversity within different root environments to the cultivation of Bt and conventional cotton varieties Li, Peng; Xue, Yong; Shi, Jialiang Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0570-9	journal	October 2018
Coupling Genetic and Chemical Microbiome Profiling Reveals Heterogeneity of Archaeome and Bacteriome in Subsurface Biofilms That Are Dominated by the Same Archaeal Species Probst, Alexander J.; Birarda, Giovanni; Holman, Hoi-Ying N. PLoS ONE, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pone.0099801	journal	June 2014
Genomic reconstruction of multiple lineages of uncultured benthic archaea suggests distinct biogeochemical roles and ecological niches The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/xj5b-0h34	text	January 2017
First genomic insights into members of a candidate bacterial phylum responsible for wastewater bulking Sekiguchi, Yuji; Ohashi, Akiko; Parks, Donovan H. PeerJ, Vol. 3 https://doi.org/10.7717/peerj.740	journal	January 2015
Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere Doud, Devin F. R.; Bowers, Robert M.; Schulz, Frederik The ISME Journal, Vol. 14, Issue 3 https://doi.org/10.1038/s41396-019-0557-y	journal	November 2019
Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction Kai-Uwe, Hinrichs,; W., Seitz, Kiley; S., Lazar, Cassandre The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/ymjj-1c73	text	January 2016
Towards quantitative viromics for both double-stranded and single-stranded DNA viruses Roux, Simon; Solonenko, Natalie E.; Dang, Vinh T. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2777	journal	January 2016
Erratum: Elevated nitrate enriches microbial functional genes for potential bioremediation of complexly contaminated sediments Xu, Meiying; Zhang, Qin; Xia, Chunyu The ISME Journal, Vol. 9, Issue 2 https://doi.org/10.1038/ismej.2014.229	journal	January 2015
Coupling Genetic and Chemical Microbiome Profiling Reveals Heterogeneity of Archaeome and Bacteriome in Subsurface Biofilms That Are Dominated by the Same Archaeal Species Probst, Alexander J.; Birarda, Giovanni; Holman, Hoi-Ying N. Universität Regensburg https://doi.org/10.5283/epub.30400	text	January 2014
Erratum: Genomic reconstruction of multiple lineages of uncultured benthic archaea suggests distinct biogeochemical roles and ecological niches Lazar, Cassandre S.; Baker, Brett J.; Seitz, Kiley W. The ISME Journal, Vol. 11, Issue 4 https://doi.org/10.1038/ismej.2017.8	journal	March 2017
Accurate and complete genomes from metagenomes Chen, Lin-Xing; Anantharaman, Karthik; Shaiber, Alon Genome Research, Vol. 30, Issue 3 https://doi.org/10.1101/gr.258640.119	journal	March 2020
Systems-based approaches to unravel multi-species microbial community functioning Abram, Florence Computational and Structural Biotechnology Journal, Vol. 13 https://doi.org/10.1016/j.csbj.2014.11.009	journal	January 2015
Discovery of anaerobic lithoheterotrophic haloarchaea, ubiquitous in hypersaline habitats Sorokin, Dimitry Y.; Messina, Enzo; Smedile, Francesco The ISME Journal, Vol. 11, Issue 5 https://doi.org/10.1038/ismej.2016.203	journal	January 2017
Erratum: Corrigendum: Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas Nature Biotechnology, Vol. 36, Issue 7 https://doi.org/10.1038/nbt0718-660a	journal	July 2018
A compendium of multi-omic sequence information from the Saanich Inlet water column Hawley, Alyse K.; Torres-Beltrán, Mónica; Zaikova, Elena Scientific Data, Vol. 4, Issue 1 https://doi.org/10.1038/sdata.2017.160	journal	October 2017
Abnormalities of Ammonia Metabolism Brown, Henry; Michelson, Paul; McDermott, William V. Postgraduate Medicine, Vol. 44, Issue 2 https://doi.org/10.1080/00325481.1968.11693350	journal	August 1968
Is there foul play in the leaf pocket? The metagenome of floating fernAzollareveals endophytes that do not fix N₂but may denitrify Dijkhuizen, Laura W.; Brouwer, Paul; Bolhuis, Henk New Phytologist, Vol. 217, Issue 1 https://doi.org/10.1111/nph.14843	journal	October 2017
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
New Perspectives on Microbial Community Distortion after Whole-Genome Amplification Probst, Alexander J.; Weinmaier, Thomas; DeSantis, Todd Z. PLOS ONE, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pone.0124158	journal	May 2015
Inter-species interconnections in acid mine drainage microbial communities Comolli, Luis R.; Banfield, Jill F. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00367	journal	July 2014
Intra- and inter-species interactions in microbial communities Comolli, Luis R. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00629	journal	November 2014
Reconstruction of Bacterial and Viral Genomes from Multiple Metagenomes Gupta, Ankit; Kumar, Sanjiv; Prasoodanan, Vishnu P. K. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00469	journal	April 2016
Carbon and Sulfur Cycling below the Chemocline in a Meromictic Lake and the Identification of a Novel Taxonomic Lineage in the FCB Superphylum, Candidatus Aegiribacteria Hamilton, Trinity L.; Bovee, Roderick J.; Sattin, Sarah R. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00598	journal	April 2016
Uncultivated archaea and associated bacteria in untapped biotopes Probst, Alexander Josef Universität Regensburg https://doi.org/10.5283/epub.30080	text	January 2015

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