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Title: Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment

Abstract

Biological features can be inferred, based on genomic data, for many microbial lineages that remain uncultured. However, cultivation is important for characterizing an organism’s physiology and testing its genome-encoded potential. Here we use single-cell genomics to infer cultivation conditions for the isolation of an ectosymbiotic Nanoarchaeota (‘Nanopusillus acidilobi’) and its host (Acidilobus, a crenarchaeote) from a terrestrial geothermal environment. The cells of ‘Nanopusillus’ are among the smallest known cellular organisms (100–300 nm). They appear to have a complete genetic information processing machinery, but lack almost all primary biosynthetic functions as well as respiration and ATP synthesis. Lastly, genomic and proteomic comparison with its distant relative, the marine Nanoarchaeum equitans illustrate an ancient, common evolutionary history of adaptation of the Nanoarchaeota to ectosymbiosis, so far unique among the Archaea.

Authors:
 [1];  [2];  [1];  [1];  [2];  [1];  [3];  [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Portland State Univ., Portland, OR (United States). Dept. of Biology
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1295113
Grant/Contract Number:  
AC05-00OR22725; SC0006654; DEB1134877
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Nanopusillus acidilobi; single-cell genomics

Citation Formats

Wurch, Louie, Giannone, Richard J., Belisle, Bernard S., Swift, Carolyn, Utturkar, Sagar, Hettich, Robert L., Reysenbach, Anna-Louise, and Podar, Mircea. Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment. United States: N. p., 2016. Web. doi:10.1038/ncomms12115.
Wurch, Louie, Giannone, Richard J., Belisle, Bernard S., Swift, Carolyn, Utturkar, Sagar, Hettich, Robert L., Reysenbach, Anna-Louise, & Podar, Mircea. Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment. United States. doi:10.1038/ncomms12115.
Wurch, Louie, Giannone, Richard J., Belisle, Bernard S., Swift, Carolyn, Utturkar, Sagar, Hettich, Robert L., Reysenbach, Anna-Louise, and Podar, Mircea. Tue . "Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment". United States. doi:10.1038/ncomms12115. https://www.osti.gov/servlets/purl/1295113.
@article{osti_1295113,
title = {Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment},
author = {Wurch, Louie and Giannone, Richard J. and Belisle, Bernard S. and Swift, Carolyn and Utturkar, Sagar and Hettich, Robert L. and Reysenbach, Anna-Louise and Podar, Mircea},
abstractNote = {Biological features can be inferred, based on genomic data, for many microbial lineages that remain uncultured. However, cultivation is important for characterizing an organism’s physiology and testing its genome-encoded potential. Here we use single-cell genomics to infer cultivation conditions for the isolation of an ectosymbiotic Nanoarchaeota (‘Nanopusillus acidilobi’) and its host (Acidilobus, a crenarchaeote) from a terrestrial geothermal environment. The cells of ‘Nanopusillus’ are among the smallest known cellular organisms (100–300 nm). They appear to have a complete genetic information processing machinery, but lack almost all primary biosynthetic functions as well as respiration and ATP synthesis. Lastly, genomic and proteomic comparison with its distant relative, the marine Nanoarchaeum equitans illustrate an ancient, common evolutionary history of adaptation of the Nanoarchaeota to ectosymbiosis, so far unique among the Archaea.},
doi = {10.1038/ncomms12115},
journal = {Nature Communications},
number = ,
volume = 7,
place = {United States},
year = {2016},
month = {7}
}

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Works referenced in this record:

Carbohydrate Metabolism in Archaea: Current Insights into Unusual Enzymes and Pathways and Their Regulation
journal, March 2014

  • Brasen, C.; Esser, D.; Rauch, B.
  • Microbiology and Molecular Biology Reviews, Vol. 78, Issue 1
  • DOI: 10.1128/MMBR.00041-13

Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer
journal, January 2012

  • Wolf, Yuri I.; Makarova, Kira S.; Yutin, Natalya
  • Biology Direct, Vol. 7, Issue 1
  • DOI: 10.1186/1745-6150-7-46

Histone and TK0471/TrmBL2 form a novel heterogeneous genome architecture in the hyperthermophilic archaeon Thermococcus kodakarensis
journal, February 2011

  • Maruyama, Hugo; Shin, Minsang; Oda, Toshiyuki
  • Molecular Biology of the Cell, Vol. 22, Issue 3
  • DOI: 10.1091/mbc.e10-08-0668

Small, Smaller, Smallest: The Origins and Evolution of Ancient Dual Symbioses in a Phloem-Feeding Insect
journal, August 2013

  • Bennett, Gordon M.; Moran, Nancy A.
  • Genome Biology and Evolution, Vol. 5, Issue 9
  • DOI: 10.1093/gbe/evt118

Isolation, Characterization, and Ecology of Sulfur-Respiring Crenarchaea Inhabiting Acid-Sulfate-Chloride-Containing Geothermal Springs in Yellowstone National Park
journal, August 2007

  • Boyd, E. S.; Jackson, R. A.; Encarnacion, G.
  • Applied and Environmental Microbiology, Vol. 73, Issue 20
  • DOI: 10.1128/AEM.01321-07

Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012


Circos: An information aesthetic for comparative genomics
journal, June 2009


Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities
journal, February 2016


Isolation of the anaerobic thermoacidophilic crenarchaeote Acidilobus saccharovorans sp. nov. and proposal of Acidilobales ord. nov., including Acidilobaceae fam. nov. and Caldisphaeraceae fam. nov.
journal, July 2009

  • Prokofeva, M. I.; Kostrikina, N. A.; Kolganova, T. V.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 12
  • DOI: 10.1099/ijs.0.010355-0

Bioenergetics of archaea: Ancient energy conserving mechanisms developed in the early history of life
journal, May 2006

  • Lewalter, Kim; Müller, Volker
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 5-6
  • DOI: 10.1016/j.bbabio.2006.04.027

Yellowstone Lake Nanoarchaeota
journal, January 2013


Genomic and evolutionary aspects of phytoplasmas
journal, January 2013


The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism
journal, October 2003

  • Waters, E.; Hohn, M. J.; Ahel, I.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 22
  • DOI: 10.1073/pnas.1735403100

Nanoarchaeota, Their Sulfolobales Host, and Nanoarchaeota Virus Distribution across Yellowstone National Park Hot Springs
journal, September 2015

  • Munson-McGee, Jacob H.; Field, Erin K.; Bateson, Mary
  • Applied and Environmental Microbiology, Vol. 81, Issue 22
  • DOI: 10.1128/AEM.01539-15

Structural Basis for a Unique ATP Synthase Core Complex from Nanoarcheaum equitans
journal, September 2015

  • Mohanty, Soumya; Jobichen, Chacko; Chichili, Vishnu Priyanka Reddy
  • Journal of Biological Chemistry, Vol. 290, Issue 45
  • DOI: 10.1074/jbc.M115.677492

Life on the edge: functional genomic response of Ignicoccus hospitalis to the presence of Nanoarchaeum equitans
journal, July 2014

  • Giannone, Richard J.; Wurch, Louie L.; Heimerl, Thomas
  • The ISME Journal, Vol. 9, Issue 1
  • DOI: 10.1038/ismej.2014.112

Rooting the Domain Archaea by Phylogenomic Analysis Supports the Foundation of the New Kingdom Proteoarchaeota
journal, December 2014

  • Petitjean, Céline; Deschamps, Philippe; López-García, Purificación
  • Genome Biology and Evolution, Vol. 7, Issue 1
  • DOI: 10.1093/gbe/evu274

DanteR: an extensible R-based tool for quantitative analysis of -omics data
journal, July 2012


Directed Culturing of Microorganisms Using Metatranscriptomics
journal, April 2011


A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont
journal, May 2002

  • Huber, Harald; Hohn, Michael J.; Rachel, Reinhard
  • Nature, Vol. 417, Issue 6884
  • DOI: 10.1038/417063a

Comparative metagenomic and rRNA microbial diversity characterization using archaeal and bacterial synthetic communities: Metagenomic and rRNA diversity characterization
journal, February 2013

  • Shakya, Migun; Quince, Christopher; Campbell, James H.
  • Environmental Microbiology, Vol. 15, Issue 6
  • DOI: 10.1111/1462-2920.12086

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

Extreme sweetness: protein glycosylation in archaea
journal, January 2013


Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling
journal, March 2015

  • Castelle, Cindy J.; Wrighton, Kelly C.; Thomas, Brian C.
  • Current Biology, Vol. 25, Issue 6
  • DOI: 10.1016/j.cub.2015.01.014

Nanoarchaeal 16S rRNA gene sequences are widely dispersed in hyperthermophilic and mesophilic halophilic environments
journal, June 2008


Acidilobus aceticus gen. nov., sp. nov., a novel anaerobic thermoacidophilic archaeon from continental hot vents in Kamchatka
journal, November 2000

  • Prokofeva, M. I.; Miroshnichenko, M. L.; Kostrikina, N. A.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 50, Issue 6
  • DOI: 10.1099/00207713-50-6-2001

Unusual biology across a group comprising more than 15% of domain Bacteria
journal, June 2015

  • Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C.
  • Nature, Vol. 523, Issue 7559
  • DOI: 10.1038/nature14486

Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle
journal, December 2014

  • He, Xuesong; McLean, Jeffrey S.; Edlund, Anna
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 1
  • DOI: 10.1073/pnas.1419038112

Sulfolobus: A new genus of sulfur-oxidizing bacteria living at low pH and high temperature
journal, January 1972

  • Brock, Thomas D.; Brock, Katherine M.; Belly, Robert T.
  • Archiv fur Mikrobiologie, Vol. 84, Issue 1, p. 54-68
  • DOI: 10.1007/BF00408082

Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics
journal, May 2008

  • Pernthaler, A.; Dekas, A. E.; Brown, C. T.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 19
  • DOI: 10.1073/pnas.0711303105

The Genome Sequence of the Crenarchaeon Acidilobus saccharovorans Supports a New Order, Acidilobales, and Suggests an Important Ecological Role in Terrestrial Acidic Hot Springs
journal, June 2010

  • Mardanov, A. V.; Svetlitchnyi, V. A.; Beletsky, A. V.
  • Applied and Environmental Microbiology, Vol. 76, Issue 16
  • DOI: 10.1128/AEM.00599-10

IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering
journal, August 2009

  • Ma, Ze-Qiang; Dasari, Surendra; Chambers, Matthew C.
  • Journal of Proteome Research, Vol. 8, Issue 8
  • DOI: 10.1021/pr900360j

Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5′- and 3′-halves
journal, February 2005

  • Randau, Lennart; Münch, Richard; Hohn, Michael J.
  • Nature, Vol. 433, Issue 7025
  • DOI: 10.1038/nature03233

Evaluation and validation of de novo and hybrid assembly techniques to derive high-quality genome sequences
journal, June 2014


Diverse uncultivated ultra-small bacterial cells in groundwater
journal, February 2015

  • Luef, Birgit; Frischkorn, Kyle R.; Wrighton, Kelly C.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7372

The universal tree of life: an update
journal, July 2015


Phosphoenolpyruvate synthase plays an essential role for glycolysis in the modified Embden-Meyerhof pathway in Thermococcus kodakarensis
journal, August 2006


Functional Convergence in Reduced Genomes of Bacterial Symbionts Spanning 200 My of Evolution
journal, January 2010

  • McCutcheon, John P.; Moran, Nancy A.
  • Genome Biology and Evolution, Vol. 2
  • DOI: 10.1093/gbe/evq055

Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013

  • Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12352

Colonization of nascent, deep-sea hydrothermal vents by a novel Archaeal and Nanoarchaeal assemblage
journal, January 2006


Nanoarchaeum equitans and Ignicoccus hospitalis: New Insights into a Unique, Intimate Association of Two Archaea
journal, December 2007

  • Jahn, U.; Gallenberger, M.; Paper, W.
  • Journal of Bacteriology, Vol. 190, Issue 5
  • DOI: 10.1128/JB.01731-07

MyriMatch:  Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis
journal, February 2007

  • Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C.
  • Journal of Proteome Research, Vol. 6, Issue 2
  • DOI: 10.1021/pr0604054

Genome-Directed Isolation of the Key Nitrogen Fixer Leptospirillum ferrodiazotrophum sp. nov. from an Acidophilic Microbial Community
journal, October 2005


Detection of 16S rDNA Sequences Representing the Novel Phylum “Nanoarchaeota”: Indication for a Wide Distribution in High Temperature Biotopes
journal, January 2002

  • Hohn, Michael J.; Hedlund, Brian P.; Huber, Harald
  • Systematic and Applied Microbiology, Vol. 25, Issue 4
  • DOI: 10.1078/07232020260517698

A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans
journal, January 2008


Involvement of Intermediate Sulfur Species in Biological Reduction of Elemental Sulfur under Acidic, Hydrothermal Conditions
journal, January 2013

  • Boyd, Eric S.; Druschel, Gregory K.
  • Applied and Environmental Microbiology, Vol. 79, Issue 6
  • DOI: 10.1128/AEM.03160-12

Proteomic Characterization of Cellular and Molecular Processes that Enable the Nanoarchaeum equitans-Ignicoccus hospitalis Relationship
journal, August 2011


Buoyant density of DNA-Hoechst 33258 (bisbenzimide) complexes in CsCl gradients: Hoechst 33258 binds to single AT base pairs
journal, April 1991


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    • DOI: 10.1073/pnas.1905179116

    Discovery of High Abundances of Aster-Like Nanoparticles in Pelagic Environments: Characterization and Dynamics
    journal, October 2019

    • Colombet, Jonathan; Billard, Hermine; Viguès, Bernard
    • Frontiers in Microbiology, Vol. 10
    • DOI: 10.3389/fmicb.2019.02376