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

Wurch, Louie; Giannone, Richard J.; Belisle, Bernard S.; Swift, Carolyn; Utturkar, Sagar; Hettich, Robert L.; Reysenbach, Anna-Louise; Podar, Mircea

doi:10.1038/ncomms12115

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

Journal Article · Tue Jul 05 00:00:00 EDT 2016 · Nature Communications

DOI:https://doi.org/10.1038/ncomms12115· OSTI ID:1295113

Wurch, Louie ^[1]; Giannone, Richard J. ^[2]; Belisle, Bernard S. ^[1]; Swift, Carolyn ^[1]; Utturkar, Sagar ^[2]; Hettich, Robert L. ^[1]; Reysenbach, Anna-Louise ^[3]; Podar, Mircea ^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Portland State Univ., Portland, OR (United States). Dept. of Biology

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.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC05-00OR22725; SC0006654

OSTI ID:: 1295113

Journal Information:: Nature Communications, Journal Name: Nature Communications Vol. 7; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (55)

Bioenergetics of archaea: Ancient energy conserving mechanisms developed in the early history of life Lewalter, Kim; Müller, Volker Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 5-6 https://doi.org/10.1016/j.bbabio.2006.04.027	journal	May 2006
The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism Waters, E.; Hohn, M. J.; Ahel, I. Proceedings of the National Academy of Sciences, Vol. 100, Issue 22 https://doi.org/10.1073/pnas.1735403100	journal	October 2003
Colonization of nascent, deep-sea hydrothermal vents by a novel Archaeal and Nanoarchaeal assemblage McCliment, Elizabeth A.; Voglesonger, Kenneth M.; O'Day, Peggy A. Environmental Microbiology, Vol. 8, Issue 1 https://doi.org/10.1111/j.1462-2920.2005.00874.x	journal	January 2006
Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park Podar, Mircea; Makarova, Kira S.; Graham, David E. Biology Direct, Vol. 8, Issue 1 https://doi.org/10.1186/1745-6150-8-9	journal	April 2013
A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans Podar, Mircea; Anderson, Iain; Makarova, Kira S. Genome Biology, Vol. 9, Issue 11 https://doi.org/10.1186/gb-2008-9-11-r158	journal	January 2008
Genomic and evolutionary aspects of phytoplasmas Oshima, Kenro; Maejima, Kensaku; Namba, Shigetou Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00230	journal	January 2013
Sulfolobus: A new genus of sulfur-oxidizing bacteria living at low pH and high temperature Brock, Thomas D.; Brock, Katherine M.; Belly, Robert T. Archiv fur Mikrobiologie, Vol. 84, Issue 1, p. 54-68 https://doi.org/10.1007/BF00408082	journal	January 1972
Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell–cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography Junglas, Benjamin; Briegel, Ariane; Burghardt, Tillmann Archives of Microbiology, Vol. 190, Issue 3 https://doi.org/10.1007/s00203-008-0402-6	journal	July 2008
Nanoarchaeal 16S rRNA gene sequences are widely dispersed in hyperthermophilic and mesophilic halophilic environments Casanueva, Ana; Galada, Ncebakazi; Baker, Gillian C. Extremophiles, Vol. 12, Issue 5 https://doi.org/10.1007/s00792-008-0170-x	journal	June 2008
Buoyant density of DNA-Hoechst 33258 (bisbenzimide) complexes in CsCl gradients: Hoechst 33258 binds to single AT base pairs Karlovsky, Petr; de Cock, Arthur W. A. M. Analytical Biochemistry, Vol. 194, Issue 1 https://doi.org/10.1016/0003-2697(91)90167-R	journal	April 1991
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
Insights into extreme thermoacidophily based on genome analysis of Picrophilus torridus and other thermoacidophilic archaea Angelov, A.; Liebl, W. Journal of Biotechnology, Vol. 126, Issue 1 https://doi.org/10.1016/j.jbiotec.2006.02.017	journal	October 2006
MyriMatch: Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C. Journal of Proteome Research, Vol. 6, Issue 2 https://doi.org/10.1021/pr0604054	journal	February 2007
IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering Ma, Ze-Qiang; Dasari, Surendra; Chambers, Matthew C. Journal of Proteome Research, Vol. 8, Issue 8 https://doi.org/10.1021/pr900360j	journal	August 2009
A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont Huber, Harald; Hohn, Michael J.; Rachel, Reinhard Nature, Vol. 417, Issue 6884 https://doi.org/10.1038/417063a	journal	May 2002
Life on the edge: functional genomic response of Ignicoccus hospitalis to the presence of Nanoarchaeum equitans Giannone, Richard J.; Wurch, Louie L.; Heimerl, Thomas The ISME Journal, Vol. 9, Issue 1 https://doi.org/10.1038/ismej.2014.112	journal	July 2014
Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5′- and 3′-halves Randau, Lennart; Münch, Richard; Hohn, Michael J. Nature, Vol. 433, Issue 7025 https://doi.org/10.1038/nature03233	journal	February 2005
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
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
Diverse uncultivated ultra-small bacterial cells in groundwater Luef, Birgit; Frischkorn, Kyle R.; Wrighton, Kelly C. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7372	journal	February 2015
Extreme sweetness: protein glycosylation in archaea Eichler, Jerry Nature Reviews Microbiology, Vol. 11, Issue 3 https://doi.org/10.1038/nrmicro2957	journal	January 2013
Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics Pernthaler, A.; Dekas, A. E.; Brown, C. T. Proceedings of the National Academy of Sciences, Vol. 105, Issue 19 https://doi.org/10.1073/pnas.0711303105	journal	May 2008
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
Structural Basis for a Unique ATP Synthase Core Complex from Nanoarcheaum equitans Mohanty, Soumya; Jobichen, Chacko; Chichili, Vishnu Priyanka Reddy Journal of Biological Chemistry, Vol. 290, Issue 45 https://doi.org/10.1074/jbc.M115.677492	journal	September 2015
Detection of 16S rDNA Sequences Representing the Novel Phylum “Nanoarchaeota”: Indication for a Wide Distribution in High Temperature Biotopes Hohn, Michael J.; Hedlund, Brian P.; Huber, Harald Systematic and Applied Microbiology, Vol. 25, Issue 4 https://doi.org/10.1078/07232020260517698	journal	January 2002
Histone and TK0471/TrmBL2 form a novel heterogeneous genome architecture in the hyperthermophilic archaeon Thermococcus kodakarensis Maruyama, Hugo; Shin, Minsang; Oda, Toshiyuki Molecular Biology of the Cell, Vol. 22, Issue 3 https://doi.org/10.1091/mbc.e10-08-0668	journal	February 2011
DanteR: an extensible R-based tool for quantitative analysis of -omics data Taverner, Tom; Karpievitch, Yuliya V.; Polpitiya, Ashoka D. Bioinformatics, Vol. 28, Issue 18 https://doi.org/10.1093/bioinformatics/bts449	journal	July 2012
Evaluation and validation of de novo and hybrid assembly techniques to derive high-quality genome sequences Utturkar, Sagar M.; Klingeman, Dawn M.; Land, Miriam L. Bioinformatics, Vol. 30, Issue 19 https://doi.org/10.1093/bioinformatics/btu391	journal	June 2014
Functional Convergence in Reduced Genomes of Bacterial Symbionts Spanning 200 My of Evolution McCutcheon, John P.; Moran, Nancy A. Genome Biology and Evolution, Vol. 2 https://doi.org/10.1093/gbe/evq055	journal	January 2010
Small, Smaller, Smallest: The Origins and Evolution of Ancient Dual Symbioses in a Phloem-Feeding Insect Bennett, Gordon M.; Moran, Nancy A. Genome Biology and Evolution, Vol. 5, Issue 9 https://doi.org/10.1093/gbe/evt118	journal	August 2013
Rooting the Domain Archaea by Phylogenomic Analysis Supports the Foundation of the New Kingdom Proteoarchaeota Petitjean, Céline; Deschamps, Philippe; López-García, Purificación Genome Biology and Evolution, Vol. 7, Issue 1 https://doi.org/10.1093/gbe/evu274	journal	December 2014
Acidilobus aceticus gen. nov., sp. nov., a novel anaerobic thermoacidophilic archaeon from continental hot vents in Kamchatka Prokofeva, M. I.; Miroshnichenko, M. L.; Kostrikina, N. A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 50, Issue 6 https://doi.org/10.1099/00207713-50-6-2001	journal	November 2000
Isolation of the anaerobic thermoacidophilic crenarchaeote Acidilobus saccharovorans sp. nov. and proposal of Acidilobales ord. nov., including Acidilobaceae fam. nov. and Caldisphaeraceae fam. nov. Prokofeva, M. I.; Kostrikina, N. A.; Kolganova, T. V. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 12 https://doi.org/10.1099/ijs.0.010355-0	journal	July 2009
Circos: An information aesthetic for comparative genomics Krzywinski, M.; Schein, J.; Birol, I. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.092759.109	journal	June 2009
Comparative metagenomic and rRNA microbial diversity characterization using archaeal and bacterial synthetic communities: Metagenomic and rRNA diversity characterization Shakya, Migun; Quince, Christopher; Campbell, James H. Environmental Microbiology, Vol. 15, Issue 6 https://doi.org/10.1111/1462-2920.12086	journal	February 2013
Phosphoenolpyruvate synthetase and pyruvate, phosphate dikinase of Thermoproteus tenax: key pieces in the puzzle of archaeal carbohydrate metabolism Tjaden, Britta; Plagens, Andre; Dorr, Christine Molecular Microbiology, Vol. 60, Issue 2 https://doi.org/10.1111/j.1365-2958.2006.05098.x	journal	April 2006
Phosphoenolpyruvate synthase plays an essential role for glycolysis in the modified Embden-Meyerhof pathway in Thermococcus kodakarensis Imanaka, Hiroyuki; Yamatsu, Atsushi; Fukui, Toshiaki Molecular Microbiology, Vol. 61, Issue 4 https://doi.org/10.1111/j.1365-2958.2006.05287.x	journal	August 2006
Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge: Microbial communities of hydrothermal vent deposits Flores, Gilberto E.; Campbell, James H.; Kirshtein, Julie D. Environmental Microbiology, Vol. 13, Issue 8 https://doi.org/10.1111/j.1462-2920.2011.02463.x	journal	March 2011
Inter-field variability in the microbial communities of hydrothermal vent deposits from a back-arc basin: Microbial communities of hydrothermal deposits Flores, G. E.; Shakya, M.; Meneghin, J. Geobiology, Vol. 10, Issue 4 https://doi.org/10.1111/j.1472-4669.2012.00325.x	journal	March 2012
Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities Xu, Qi; Resch, Michael G.; Podkaminer, Kara Science Advances, Vol. 2, Issue 2 https://doi.org/10.1126/sciadv.1501254	journal	February 2016
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
The Genome Sequence of the Crenarchaeon Acidilobus saccharovorans Supports a New Order, Acidilobales, and Suggests an Important Ecological Role in Terrestrial Acidic Hot Springs Mardanov, A. V.; Svetlitchnyi, V. A.; Beletsky, A. V. Applied and Environmental Microbiology, Vol. 76, Issue 16 https://doi.org/10.1128/AEM.00599-10	journal	June 2010
Isolation, Characterization, and Ecology of Sulfur-Respiring Crenarchaea Inhabiting Acid-Sulfate-Chloride-Containing Geothermal Springs in Yellowstone National Park Boyd, E. S.; Jackson, R. A.; Encarnacion, G. Applied and Environmental Microbiology, Vol. 73, Issue 20 https://doi.org/10.1128/AEM.01321-07	journal	August 2007
Nanoarchaeota, Their Sulfolobales Host, and Nanoarchaeota Virus Distribution across Yellowstone National Park Hot Springs Munson-McGee, Jacob H.; Field, Erin K.; Bateson, Mary Applied and Environmental Microbiology, Vol. 81, Issue 22 https://doi.org/10.1128/AEM.01539-15	journal	September 2015
Predominant Acidilobus-Like Populations from Geothermal Environments in Yellowstone National Park Exhibit Similar Metabolic Potential in Different Hypoxic Microbial Communities Jay, Z. J.; Rusch, D. B.; Tringe, S. G. Applied and Environmental Microbiology, Vol. 80, Issue 1 https://doi.org/10.1128/AEM.02860-13	journal	October 2013
Involvement of Intermediate Sulfur Species in Biological Reduction of Elemental Sulfur under Acidic, Hydrothermal Conditions Boyd, Eric S.; Druschel, Gregory K. Applied and Environmental Microbiology, Vol. 79, Issue 6 https://doi.org/10.1128/AEM.03160-12	journal	January 2013
Genome-Directed Isolation of the Key Nitrogen Fixer Leptospirillum ferrodiazotrophum sp. nov. from an Acidophilic Microbial Community Tyson, G. W.; Lo, I.; Baker, B. J. Applied and Environmental Microbiology, Vol. 71, Issue 10 https://doi.org/10.1128/AEM.71.10.6319-6324.2005	journal	October 2005
Nanoarchaeum equitans and Ignicoccus hospitalis: New Insights into a Unique, Intimate Association of Two Archaea Jahn, U.; Gallenberger, M.; Paper, W. Journal of Bacteriology, Vol. 190, Issue 5 https://doi.org/10.1128/JB.01731-07	journal	December 2007
Carbohydrate Metabolism in Archaea: Current Insights into Unusual Enzymes and Pathways and Their Regulation Brasen, C.; Esser, D.; Rauch, B. Microbiology and Molecular Biology Reviews, Vol. 78, Issue 1 https://doi.org/10.1128/MMBR.00041-13	journal	March 2014
Directed Culturing of Microorganisms Using Metatranscriptomics Bomar, Lindsey; Maltz, Michele; Colston, Sophie mBio, Vol. 2, Issue 2 https://doi.org/10.1128/mBio.00012-11	journal	April 2011
Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer Wolf, Yuri I.; Makarova, Kira S.; Yutin, Natalya Biology Direct, Vol. 7, Issue 1 https://doi.org/10.1186/1745-6150-7-46	journal	January 2012
Proteomic Characterization of Cellular and Molecular Processes that Enable the Nanoarchaeum equitans-Ignicoccus hospitalis Relationship Giannone, Richard J.; Huber, Harald; Karpinets, Tatiana PLoS ONE, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pone.0022942	journal	August 2011
Yellowstone Lake Nanoarchaeota Clingenpeel, Scott; Kan, Jinjun; Macur, Richard E. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00274	journal	January 2013
The universal tree of life: an update Forterre, Patrick Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00717	journal	July 2015

Cited By (6)

The trajectory of microbial single-cell sequencing Woyke, Tanja; Doud, Devin F. R.; Schulz, Frederik Nature Methods, Vol. 14, Issue 11 https://doi.org/10.1038/nmeth.4469	journal	October 2017
Genome size evolution in the Archaea Kellner, Siri; Spang, Anja; Offre, Pierre Emerging Topics in Life Sciences, Vol. 2, Issue 4 https://doi.org/10.1042/etls20180021	journal	November 2018
Unexpected host dependency of Antarctic Nanohaloarchaeota Hamm, Joshua N.; Erdmann, Susanne; Eloe-Fadrosh, Emiley A. Proceedings of the National Academy of Sciences, Vol. 116, Issue 29 https://doi.org/10.1073/pnas.1905179116	journal	June 2019
The multi-omics promise in context: from sequence to microbial isolate Gutleben, Johanna; Chaib De Mares, Maryam; van Elsas, Jan Dirk Critical Reviews in Microbiology, Vol. 44, Issue 2 https://doi.org/10.1080/1040841x.2017.1332003	journal	May 2017
Assembling metagenomes, one community at a time van der Walt, Andries Johannes; van Goethem, Marc Warwick; Ramond, Jean-Baptiste BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-3918-9	journal	July 2017
Characterisation of a stable laboratory co-culture of acidophilic nanoorganisms Krause, S.; Bremges, A.; Münch, P. C. Karlsruhe https://doi.org/10.5445/ir/1000071504	text	January 2017

Similar Records

A new symbiotic nanoarchaeote (Candidatus Nanoclepta minutus) and its host (Zestosphaera tikiterensis gen. nov., sp. nov.) from a New Zealand hot spring

Journal Article · Wed Aug 15 20:00:00 EDT 2018 · Systematic and Applied Microbiology · OSTI ID:1470848

Candidatus Nanopusillus

Book · Thu Jun 29 00:00:00 EDT 2023 · Bergey's Manual of Systematics of Archaea and Bacteria · OSTI ID:1991694

Insights into archaeal evolution and symbiosis from the genomes of a Nanoarchaeon and its crenarchaeal host from Yellowstone National Park

Journal Article · Mon Dec 31 23:00:00 EST 2012 · Biology Direct · OSTI ID:1118740

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Nanopusillus acidilobi
single-cell genomics

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

Citation Formats

References (55)

Cited By (6)

Similar Records

Related Subjects