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Title: Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs

Abstract

Analysis of the increasing wealth of metagenomic data collected from diverse environments can lead to the discovery of novel branches on the tree of life. Here we analyse 5.2 Tb of metagenomic data collected globally to discover a novel bacterial phylum ('Candidatus Kryptonia') found exclusively in higherature pH-neutral geothermal springs. This lineage had remained hidden as a taxonomic 'blind spot' because of mismatches in the primers commonly used for ribosomal gene surveys. Genome reconstruction from metagenomic data combined with single-cell genomics results in several high-quality genomes representing four genera from the new phylum. Metabolic reconstruction indicates a heterotrophic lifestyle with conspicuous nutritional deficiencies, suggesting the need for metabolic complementarity with other microbes. Co-occurrence patterns identifies a number of putative partners, including an uncultured Armatimonadetes lineage. The discovery of Kryptonia within previously studied geothermal springs underscores the importance of globally sampled metagenomic data in detection of microbial novelty, and highlights the extraordinary diversity of microbial life still awaiting discovery.

Authors:
 [1];  [1];  [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [1];  [1];  [1];  [4];  [10];  [1];  [1];  [1]
  1. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. Univ. of Calgary, AB (Canada)
  3. Univ. of Nevada, Las Vegas, NV (United States)
  4. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  5. Geological Survey of Canada, Calgary, AB (Canada)
  6. McMaster Univ., Hamilton, ON (Canada)
  7. Miami Univ., Oxford, OH (United States)
  8. Univ. of Alaska, Anchorage, AK (United States)
  9. Sun Yat-Sen Univ., Guangzhou, (China)
  10. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1467799
Alternate Identifier(s):
OSTI ID: 1379050
Report Number(s):
LLNL-JRNL-737993
Journal ID: ISSN 2041-1723; 891150
Grant/Contract Number:  
AC52-07NA27344; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal Issue: na; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Biodiversity; Metagenomics

Citation Formats

Eloe-Fadrosh, Emiley A., Paez-Espino, David, Jarett, Jessica, Dunfield, Peter F., Hedlund, Brian P., Dekas, Anne E., Grasby, Stephen E., Brady, Allyson L., Dong, Hailiang, Briggs, Brandon R., Li, Wen-Jun, Goudeau, Danielle, Malmstrom, Rex, Pati, Amrita, Pett-Ridge, Jennifer, Rubin, Edward M., Woyke, Tanja, Kyrpides, Nikos C., and Ivanova, Natalia N. Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs. United States: N. p., 2016. Web. doi:10.1038/ncomms10476.
Eloe-Fadrosh, Emiley A., Paez-Espino, David, Jarett, Jessica, Dunfield, Peter F., Hedlund, Brian P., Dekas, Anne E., Grasby, Stephen E., Brady, Allyson L., Dong, Hailiang, Briggs, Brandon R., Li, Wen-Jun, Goudeau, Danielle, Malmstrom, Rex, Pati, Amrita, Pett-Ridge, Jennifer, Rubin, Edward M., Woyke, Tanja, Kyrpides, Nikos C., & Ivanova, Natalia N. Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs. United States. https://doi.org/10.1038/ncomms10476
Eloe-Fadrosh, Emiley A., Paez-Espino, David, Jarett, Jessica, Dunfield, Peter F., Hedlund, Brian P., Dekas, Anne E., Grasby, Stephen E., Brady, Allyson L., Dong, Hailiang, Briggs, Brandon R., Li, Wen-Jun, Goudeau, Danielle, Malmstrom, Rex, Pati, Amrita, Pett-Ridge, Jennifer, Rubin, Edward M., Woyke, Tanja, Kyrpides, Nikos C., and Ivanova, Natalia N. Wed . "Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs". United States. https://doi.org/10.1038/ncomms10476. https://www.osti.gov/servlets/purl/1467799.
@article{osti_1467799,
title = {Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs},
author = {Eloe-Fadrosh, Emiley A. and Paez-Espino, David and Jarett, Jessica and Dunfield, Peter F. and Hedlund, Brian P. and Dekas, Anne E. and Grasby, Stephen E. and Brady, Allyson L. and Dong, Hailiang and Briggs, Brandon R. and Li, Wen-Jun and Goudeau, Danielle and Malmstrom, Rex and Pati, Amrita and Pett-Ridge, Jennifer and Rubin, Edward M. and Woyke, Tanja and Kyrpides, Nikos C. and Ivanova, Natalia N.},
abstractNote = {Analysis of the increasing wealth of metagenomic data collected from diverse environments can lead to the discovery of novel branches on the tree of life. Here we analyse 5.2 Tb of metagenomic data collected globally to discover a novel bacterial phylum ('Candidatus Kryptonia') found exclusively in higherature pH-neutral geothermal springs. This lineage had remained hidden as a taxonomic 'blind spot' because of mismatches in the primers commonly used for ribosomal gene surveys. Genome reconstruction from metagenomic data combined with single-cell genomics results in several high-quality genomes representing four genera from the new phylum. Metabolic reconstruction indicates a heterotrophic lifestyle with conspicuous nutritional deficiencies, suggesting the need for metabolic complementarity with other microbes. Co-occurrence patterns identifies a number of putative partners, including an uncultured Armatimonadetes lineage. The discovery of Kryptonia within previously studied geothermal springs underscores the importance of globally sampled metagenomic data in detection of microbial novelty, and highlights the extraordinary diversity of microbial life still awaiting discovery.},
doi = {10.1038/ncomms10476},
journal = {Nature Communications},
number = na,
volume = 7,
place = {United States},
year = {Wed Jan 27 00:00:00 EST 2016},
month = {Wed Jan 27 00:00:00 EST 2016}
}

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journal, June 2019

  • Guo, M. Y.; Hou, C. J.; Bian, M. H.
  • Journal of Applied Microbiology, Vol. 127, Issue 3
  • DOI: 10.1111/jam.14279

Evaluation of prokaryotic diversity of five hot springs in Eritrea
journal, September 2017

  • Ghilamicael, Amanuel M.; Budambula, Nancy L. M.; Anami, Sylvester E.
  • BMC Microbiology, Vol. 17, Issue 1
  • DOI: 10.1186/s12866-017-1113-4

Functional and taxonomic classification of a greenhouse water drain metagenome
journal, October 2018

  • López-Leal, Gamaliel; Cornejo-Granados, Fernanda; Hurtado-Ramírez, Juan Manuel
  • Standards in Genomic Sciences, Vol. 13, Issue 1
  • DOI: 10.1186/s40793-018-0326-y

Genomic Description of ‘Candidatus Abyssubacteria,’ a Novel Subsurface Lineage Within the Candidate Phylum Hydrogenedentes
journal, August 2018


Living on the edge: biofilms developing in oscillating environmental conditions
text, January 2019


Freiburg RNA tools: a central online resource for RNA-focused research and teaching.
text, January 2018

  • Raden, Martin; Ali, Syed M.; Alkhnbashi, Omer S.
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.32049

Kryptonium thompsonii sp. nov. gen. nov.
text, January 2022


Exemplar Abstract for Kryptobacter tengchongensis Eloe-Fadrosh et al. 2016.
dataset, January 2019


Exemplar Abstract for Thermokryptus mobilis Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Kryptonia Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Incertae sedis 386 Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Kryptonium Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Kryptobacter Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Kryptobacter tengchongensis Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Thermokryptus Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Thermokryptus mobilis Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Chrysopegis (sic) Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Chrysopegis kryptomonas (sic) Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Chryseopegocella corrig. Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Chryseopegocella kryptomonas corrig. Eloe-Fadrosh et al. 2016.
dataset, January 2019


Nomenclature Abstract for Kryptonium thompsonii corrig. Eloe-Fadrosh et al. 2016.
dataset, January 2019


Taxon Abstract for the Domain Archaea
dataset, January 1990


Taxonomic Abstract for the class Incertae sedis 384 Eloe-Fadrosh et al. 2016
dataset, January 2019


Taxonomic Abstract for the species.
dataset, January 2019


Taxonomic Abstract for the genera.
dataset, January 2019


Taxonomic Abstract for the species.
dataset, January 2019


Taxonomic Abstract for the species.
dataset, January 2019


Unraveling the microbial and functional diversity of Coamo thermal spring in Puerto Rico using metagenomic library generation and shotgun sequencing
journal, March 2017


1,003 reference genomes of bacterial and archaeal isolates expand coverage of the tree of life
journal, June 2017

  • Mukherjee, Supratim; Seshadri, Rekha; Varghese, Neha J.
  • Nature Biotechnology, Vol. 35, Issue 7
  • DOI: 10.1038/nbt.3886

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

Novel prosthecate bacteria from the candidate phylum Acetothermia
journal, June 2018

  • Hao, Liping; McIlroy, Simon Jon; Kirkegaard, Rasmus Hansen
  • The ISME Journal, Vol. 12, Issue 9
  • DOI: 10.1038/s41396-018-0187-9

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


Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes
journal, July 2019


Analyzing large scale genomic data on the cloud with Sparkhit
journal, December 2017


The Evolution of Reverse Gyrase Suggests a Nonhyperthermophilic Last Universal Common Ancestor
journal, September 2019

  • Catchpole, Ryan J.; Forterre, Patrick
  • Molecular Biology and Evolution, Vol. 36, Issue 12
  • DOI: 10.1093/molbev/msz180

IMG/M: integrated genome and metagenome comparative data analysis system
journal, October 2016

  • Chen, I-Min A.; Markowitz, Victor M.; Chu, Ken
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw929

Genomes OnLine Database (GOLD) v.6: data updates and feature enhancements
journal, October 2016

  • Mukherjee, Supratim; Stamatis, Dimitri; Bertsch, Jon
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw992

The MAR databases: development and implementation of databases specific for marine metagenomics
journal, November 2017

  • Klemetsen, Terje; Raknes, Inge A.; Fu, Juan
  • Nucleic Acids Research, Vol. 46, Issue D1
  • DOI: 10.1093/nar/gkx1036

Novel prosthecate bacteria from the candidate phylum Acetothermia revealed by culture-independent genomics and advanced microscopy
journal, October 2017

  • Hao, Li-Ping; Mcllroy, Simon Jon; Kirkegaard, Rasmus Hansen
  • The ISME Journal
  • DOI: 10.1101/207811

Bioremediation at a global scale: from the test tube to planet Earth
journal, August 2016

  • de Lorenzo, Víctor; Marlière, Philippe; Solé, Ricard
  • Microbial Biotechnology, Vol. 9, Issue 5
  • DOI: 10.1111/1751-7915.12399

Functional and taxonomic classification of a greenhouse water drain metagenome
journal, October 2018

  • López-Leal, Gamaliel; Cornejo-Granados, Fernanda; Hurtado-Ramírez, Juan Manuel
  • Standards in Genomic Sciences, Vol. 13, Issue 1
  • DOI: 10.1186/s40793-018-0326-y

Freiburg RNA tools: a central online resource for RNA-focused research and teaching.
text, January 2018

  • Raden, Martin; Ali, Syed M.; Alkhnbashi, Omer S.
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.32049

Taxonomic Abstract for the genera.
dataset, January 2019