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Title: Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment

Abstract

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.

Authors:
 [1];  [1];  [1];  [1];  [2];  [3];  [4];  [2];  [5];  [6]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division
  3. Univ. of California, Davis, CA (United States). UC Davis Genome Center
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics Division
  5. Univ. of California, Davis, CA (United States). UC Davis Genome Center. Dept. of Evolution and Ecology. Dept. of Medical Microbiology and Immunology
  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
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1407195
Grant/Contract Number:  
AC02-05CH11231; SC0004733
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 4; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; microbial communities; phylogenomics

Citation Formats

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., and Banfield, Jillian F. Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment. United States: N. p., 2013. Web. doi:10.1038/ncomms3120.
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. Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment. United States. https://doi.org/10.1038/ncomms3120
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., and Banfield, Jillian F. Tue . "Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment". United States. https://doi.org/10.1038/ncomms3120. https://www.osti.gov/servlets/purl/1407195.
@article{osti_1407195,
title = {Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment},
author = {Castelle, Cindy J. and Hug, Laura A. and Wrighton, Kelly C. and Thomas, Brian C. and Williams, Kenneth H. and Wu, Dongying and Tringe, Susannah G. and Singer, Steven W. and Eisen, Jonathan A. and Banfield, Jillian F.},
abstractNote = {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.},
doi = {10.1038/ncomms3120},
journal = {Nature Communications},
number = ,
volume = 4,
place = {United States},
year = {Tue Aug 27 00:00:00 EDT 2013},
month = {Tue Aug 27 00:00:00 EDT 2013}
}

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Cited by: 145 works
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  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.02101

Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer
journal, January 2017

  • Jewell, Talia N. M.; Karaoz, Ulas; Bill, Markus
  • Frontiers in Microbiology, Vol. 8, Article No. 40
  • DOI: 10.3389/fmicb.2017.00040

High-Throughput Sequencing Analysis of the Actinobacterial Spatial Diversity in Moonmilk Deposits
journal, March 2018


Crowdsourcing the identification of organisms: A case-study of iSpot
journal, February 2015


Spatial variations of microbial communities in abyssal and hadal sediments across the Challenger Deep
journal, January 2019


RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria
journal, May 2016

  • Wrighton, Kelly C.; Castelle, Cindy J.; Varaljay, Vanessa A.
  • The ISME Journal, Vol. 10, Issue 11
  • DOI: 10.1038/ismej.2016.53

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

Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016

  • Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13219

Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface
journal, November 2014

  • Probst, Alexander J.; Weinmaier, Thomas; Raymann, Kasie
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms6497

Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria
journal, January 2019

  • Matheus Carnevali, Paula B.; Schulz, Frederik; Castelle, Cindy J.
  • Nature Communications, Vol. 10, Issue 1
  • DOI: 10.1038/s41467-018-08246-y

Influence of pH on the balance between methanogenesis and iron reduction
journal, November 2018

  • Marquart, Kyle A.; Haller, Ben R.; Paper, Janet M.
  • Geobiology, Vol. 17, Issue 2
  • DOI: 10.1111/gbi.12320

First genomic insights into members of a candidate bacterial phylum responsible for wastewater bulking
journal, January 2015

  • Sekiguchi, Yuji; Ohashi, Akiko; Parks, Donovan H.
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.740

Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere
journal, November 2019


Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction
text, January 2016

  • Kai-Uwe, Hinrichs,; W., Seitz, Kiley; S., Lazar, Cassandre
  • The University of North Carolina at Chapel Hill University Libraries
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Towards quantitative viromics for both double-stranded and single-stranded DNA viruses
journal, January 2016


Erratum: Elevated nitrate enriches microbial functional genes for potential bioremediation of complexly contaminated sediments
journal, January 2015


Erratum: Genomic reconstruction of multiple lineages of uncultured benthic archaea suggests distinct biogeochemical roles and ecological niches
journal, March 2017

  • Lazar, Cassandre S.; Baker, Brett J.; Seitz, Kiley W.
  • The ISME Journal, Vol. 11, Issue 4
  • DOI: 10.1038/ismej.2017.8

Accurate and complete genomes from metagenomes
journal, March 2020

  • Chen, Lin-Xing; Anantharaman, Karthik; Shaiber, Alon
  • Genome Research, Vol. 30, Issue 3
  • DOI: 10.1101/gr.258640.119

Systems-based approaches to unravel multi-species microbial community functioning
journal, January 2015


Discovery of anaerobic lithoheterotrophic haloarchaea, ubiquitous in hypersaline habitats
journal, January 2017

  • Sorokin, Dimitry Y.; Messina, Enzo; Smedile, Francesco
  • The ISME Journal, Vol. 11, Issue 5
  • DOI: 10.1038/ismej.2016.203

RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria
journal, May 2016

  • Wrighton, Kelly C.; Castelle, Cindy J.; Varaljay, Vanessa A.
  • The ISME Journal, Vol. 10, Issue 11
  • DOI: 10.1038/ismej.2016.53

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

SAR11 bacteria linked to ocean anoxia and nitrogen loss
journal, August 2016

  • Tsementzi, Despina; Wu, Jieying; Deutsch, Samuel
  • Nature, Vol. 536, Issue 7615
  • DOI: 10.1038/nature19068

Erratum: Corrigendum: Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea
journal, July 2018

  • Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas
  • Nature Biotechnology, Vol. 36, Issue 7
  • DOI: 10.1038/nbt0718-660a

Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016

  • Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13219

Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface
journal, November 2014

  • Probst, Alexander J.; Weinmaier, Thomas; Raymann, Kasie
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms6497

Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere
journal, November 2019


A compendium of multi-omic sequence information from the Saanich Inlet water column
journal, October 2017

  • Hawley, Alyse K.; Torres-Beltrán, Mónica; Zaikova, Elena
  • Scientific Data, Vol. 4, Issue 1
  • DOI: 10.1038/sdata.2017.160

Unusual respiratory capacity and nitrogen metabolism in a Parcubacterium (OD1) of the Candidate Phyla Radiation
journal, January 2017

  • Castelle, Cindy J.; Brown, Christopher T.; Thomas, Brian C.
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep40101

Abnormalities of Ammonia Metabolism
journal, August 1968


Impact of hydrologic boundaries on microbial planktonic and biofilm communities in shallow terrestrial subsurface environments
journal, September 2018

  • Smith, H. J.; Zelaya, A. J.; De León, K. B.
  • FEMS Microbiology Ecology, Vol. 94, Issue 12
  • DOI: 10.1093/femsec/fiy191

Is there foul play in the leaf pocket? The metagenome of floating fernAzollareveals endophytes that do not fix N2but may denitrify
journal, October 2017

  • Dijkhuizen, Laura W.; Brouwer, Paul; Bolhuis, Henk
  • New Phytologist, Vol. 217, Issue 1
  • DOI: 10.1111/nph.14843

Metagenomic analysis of microbial community and function involved in cd-contaminated soil
journal, February 2018


Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria
journal, April 2015


Recovering complete and draft population genomes from metagenome datasets
journal, March 2016


New Perspectives on Microbial Community Distortion after Whole-Genome Amplification
journal, May 2015


Snowmelt Induced Hydrologic Perturbations Drive Dynamic Microbiological and Geochemical Behaviors across a Shallow Riparian Aquifer
journal, May 2016

  • Danczak, Robert E.; Yabusaki, Steven B.; Williams, Kenneth H.
  • Frontiers in Earth Science, Vol. 4
  • DOI: 10.3389/feart.2016.00057

Inter-species interconnections in acid mine drainage microbial communities
journal, July 2014


Intra- and inter-species interactions in microbial communities
journal, November 2014


Groundwater Isolation Governs Chemistry and Microbial Community Structure along Hydrologic Flowpaths
journal, December 2015


Fungi Contribute Critical but Spatially Varying Roles in Nitrogen and Carbon Cycling in Acid Mine Drainage
journal, March 2016

  • Mosier, Annika C.; Miller, Christopher S.; Frischkorn, Kyle R.
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00238

Reconstruction of Bacterial and Viral Genomes from Multiple Metagenomes
journal, April 2016

  • Gupta, Ankit; Kumar, Sanjiv; Prasoodanan, Vishnu P. K.
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00469

Genomic and Transcriptomic Resolution of Organic Matter Utilization Among Deep-Sea Bacteria in Guaymas Basin Hydrothermal Plumes
journal, July 2016


Stable and Variable Parts of Microbial Community in Siberian Deep Subsurface Thermal Aquifer System Revealed in a Long-Term Monitoring Study
journal, December 2016

  • Frank, Yulia A.; Kadnikov, Vitaly V.; Gavrilov, Sergey N.
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.02101

Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer
journal, January 2017

  • Jewell, Talia N. M.; Karaoz, Ulas; Bill, Markus
  • Frontiers in Microbiology, Vol. 8, Article No. 40
  • DOI: 10.3389/fmicb.2017.00040

High-Throughput Sequencing Analysis of the Actinobacterial Spatial Diversity in Moonmilk Deposits
journal, March 2018


Crowdsourcing the identification of organisms: A case-study of iSpot
journal, February 2015


Uncultivated archaea and associated bacteria in untapped biotopes
text, January 2015


Towards quantitative viromics for both double-stranded and single-stranded DNA viruses
journal, January 2016


Spatial variations of microbial communities in abyssal and hadal sediments across the Challenger Deep
journal, January 2019


First genomic insights into members of a candidate bacterial phylum responsible for wastewater bulking
journal, January 2015

  • Sekiguchi, Yuji; Ohashi, Akiko; Parks, Donovan H.
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.740