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Title: Carboxydotrophy potential of uncultivated Hydrothermarchaeota from the subseafloor crustal biosphere

Abstract

The exploration of Earth's terrestrial subsurface biosphere has led to the discovery of several new archaeal lineages of evolutionary significance. Similarly, the deep subseafloor crustal biosphere also harbors many unique, uncultured archaeal taxa, including those belonging to Candidatus Hydrothermarchaeota, formerly known as Marine Benthic Group-E. Recently, Hydrothermarchaeota was identified as an abundant lineage of Juan de Fuca Ridge flank crustal fluids, suggesting its adaptation to this extreme environment. Through the investigation of single-cell and metagenome-assembled genomes, we provide insight into the lineage's evolutionary history and metabolic potential. Phylogenomic analysis reveals the Hydrothermarchaeota to be an early-branching archaeal phylum, branching between the superphylum DPANN, Euryarchaeota, and Asgard lineages. Hydrothermarchaeota genomes suggest a potential for dissimilative and assimilative carbon monoxide oxidation (carboxydotrophy), as well as sulfate and nitrate reduction. There is also a prevalence of chemotaxis and motility genes, indicating adaptive strategies for this nutrient-limited fluid-rock environment. These findings provide the first genomic interpretations of the Hydrothermarchaeota phylum and highlight the anoxic, hot, deep marine crustal biosphere as an important habitat for understanding the evolution of early life.

Authors:
 [1]; ORCiD logo [2];  [3]; ORCiD logo [4];  [3];  [5]; ORCiD logo [4]
  1. Bigelow Laboratory for Ocean Sciences, East Boothbay, ME (United States); Hartwick College, Oneonta, NY (United States)
  2. Univ. of Southern California, Los Angeles, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of Hawaii, Honolulu, HI (United States)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Bigelow Laboratory for Ocean Sciences, East Boothbay, ME (United States)
  5. Univ. of Hawaii, Honolulu, HI (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF)
OSTI Identifier:
1572825
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 13; Journal Issue: 6; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Carr, Stephanie A., Jungbluth, Sean P., Eloe-Fadrosh, Emiley A., Stepanauskas, Ramunas, Woyke, Tanja, Rappé, Michael S., and Orcutt, Beth N. Carboxydotrophy potential of uncultivated Hydrothermarchaeota from the subseafloor crustal biosphere. United States: N. p., 2019. Web. doi:10.1038/s41396-019-0352-9.
Carr, Stephanie A., Jungbluth, Sean P., Eloe-Fadrosh, Emiley A., Stepanauskas, Ramunas, Woyke, Tanja, Rappé, Michael S., & Orcutt, Beth N. Carboxydotrophy potential of uncultivated Hydrothermarchaeota from the subseafloor crustal biosphere. United States. doi:10.1038/s41396-019-0352-9.
Carr, Stephanie A., Jungbluth, Sean P., Eloe-Fadrosh, Emiley A., Stepanauskas, Ramunas, Woyke, Tanja, Rappé, Michael S., and Orcutt, Beth N. Thu . "Carboxydotrophy potential of uncultivated Hydrothermarchaeota from the subseafloor crustal biosphere". United States. doi:10.1038/s41396-019-0352-9. https://www.osti.gov/servlets/purl/1572825.
@article{osti_1572825,
title = {Carboxydotrophy potential of uncultivated Hydrothermarchaeota from the subseafloor crustal biosphere},
author = {Carr, Stephanie A. and Jungbluth, Sean P. and Eloe-Fadrosh, Emiley A. and Stepanauskas, Ramunas and Woyke, Tanja and Rappé, Michael S. and Orcutt, Beth N.},
abstractNote = {The exploration of Earth's terrestrial subsurface biosphere has led to the discovery of several new archaeal lineages of evolutionary significance. Similarly, the deep subseafloor crustal biosphere also harbors many unique, uncultured archaeal taxa, including those belonging to Candidatus Hydrothermarchaeota, formerly known as Marine Benthic Group-E. Recently, Hydrothermarchaeota was identified as an abundant lineage of Juan de Fuca Ridge flank crustal fluids, suggesting its adaptation to this extreme environment. Through the investigation of single-cell and metagenome-assembled genomes, we provide insight into the lineage's evolutionary history and metabolic potential. Phylogenomic analysis reveals the Hydrothermarchaeota to be an early-branching archaeal phylum, branching between the superphylum DPANN, Euryarchaeota, and Asgard lineages. Hydrothermarchaeota genomes suggest a potential for dissimilative and assimilative carbon monoxide oxidation (carboxydotrophy), as well as sulfate and nitrate reduction. There is also a prevalence of chemotaxis and motility genes, indicating adaptive strategies for this nutrient-limited fluid-rock environment. These findings provide the first genomic interpretations of the Hydrothermarchaeota phylum and highlight the anoxic, hot, deep marine crustal biosphere as an important habitat for understanding the evolution of early life.},
doi = {10.1038/s41396-019-0352-9},
journal = {The ISME Journal},
number = 6,
volume = 13,
place = {United States},
year = {2019},
month = {2}
}

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Works referenced in this record:

Anvi’o: an advanced analysis and visualization platform for ‘omics data
journal, January 2015

  • Eren, A. Murat; Esen, Özcan C.; Quince, Christopher
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.1319

Asgard archaea illuminate the origin of eukaryotic cellular complexity
journal, January 2017

  • Zaremba-Niedzwiedzka, Katarzyna; Caceres, Eva F.; Saw, Jimmy H.
  • Nature, Vol. 541, Issue 7637
  • DOI: 10.1038/nature21031

Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics
journal, October 2015


The Archaellum: An Update on the Unique Archaeal Motility Structure
journal, April 2018


The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4)
journal, October 2015

  • Huntemann, Marcel; Ivanova, Natalia N.; Mavromatis, Konstantinos
  • Standards in Genomic Sciences, Vol. 10, Issue 1
  • DOI: 10.1186/s40793-015-0077-y

Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea
journal, August 2017

  • Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas
  • Nature Biotechnology, Vol. 35, Issue 8
  • DOI: 10.1038/nbt.3893

Subseafloor Ocean Crust Microbial Observatories: Development of FLOCS (FLow-through Osmo Colonization System) and Evaluation of Borehole Construction Materials
journal, February 2010

  • Orcutt, Beth; Wheat, C. Geoffrey; Edwards, Katrina J.
  • Geomicrobiology Journal, Vol. 27, Issue 2
  • DOI: 10.1080/01490450903456772

Ultrastructural Characterization of the Lower Motor System in a Mouse Model of Krabbe Disease
journal, December 2016


Microbial Ecology of the Dark Ocean above, at, and below the Seafloor
journal, June 2011

  • Orcutt, B. N.; Sylvan, J. B.; Knab, N. J.
  • Microbiology and Molecular Biology Reviews, Vol. 75, Issue 2
  • DOI: 10.1128/MMBR.00039-10

New Mode of Energy Metabolism in the Seventh Order of Methanogens as Revealed by Comparative Genome Analysis of “Candidatus Methanoplasma termitum”
journal, December 2014

  • Lang, Kristina; Schuldes, Jörg; Klingl, Andreas
  • Applied and Environmental Microbiology, Vol. 81, Issue 4
  • DOI: 10.1128/AEM.03389-14

Seawater recharge into oceanic crust: IODP Exp 327 Site U1363 Grizzly Bare outcrop: SEAWATER RECHARGE INTO BASALTIC CRUST
journal, June 2013

  • Wheat, C. Geoffrey; Hulme, Samuel M.; Fisher, Andrew T.
  • Geochemistry, Geophysics, Geosystems, Vol. 14, Issue 6
  • DOI: 10.1002/ggge.20131

Integrative modeling of gene and genome evolution roots the archaeal tree of life
journal, May 2017

  • Williams, Tom A.; Szöllősi, Gergely J.; Spang, Anja
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 23
  • DOI: 10.1073/pnas.1618463114

Dissolved hydrogen and methane in the oceanic basaltic biosphere
journal, November 2014


FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Trade-Offs of Chemotactic Foraging in Turbulent Water
journal, November 2012


The primary divisions of life: a phylogenomic approach employing composition-heterogeneous methods
journal, August 2009

  • Foster, Peter G.; Cox, Cymon J.; Embley, T. Martin
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 364, Issue 1527
  • DOI: 10.1098/rstb.2009.0034

Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life
journal, August 2017


Mapping the Tree of Life: Progress and Prospects
journal, November 2009


Microbial Community in Black Rust Exposed to Hot Ridge Flank Crustal Fluids
journal, August 2006

  • Nakagawa, S.; Inagaki, F.; Suzuki, Y.
  • Applied and Environmental Microbiology, Vol. 72, Issue 10
  • DOI: 10.1128/AEM.01238-06

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


Marsarchaeota are an aerobic archaeal lineage abundant in geothermal iron oxide microbial mats
journal, May 2018


A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life
journal, August 2018

  • Parks, Donovan H.; Chuvochina, Maria; Waite, David W.
  • Nature Biotechnology, Vol. 36, Issue 10
  • DOI: 10.1038/nbt.4229

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

In situ click chemistry generation of cyclooxygenase-2 inhibitors
journal, February 2017


Evidence for Microbial Carbon and Sulfur Cycling in Deeply Buried Ridge Flank Basalt
journal, March 2013


Geochemical bioenergetics during low-temperature serpentinization: An example from the Samail ophiolite, Sultanate of Oman: Serpentinization Bioenergetics
journal, July 2017

  • Canovas, Peter A.; Hoehler, Tori; Shock, Everett L.
  • Journal of Geophysical Research: Biogeosciences, Vol. 122, Issue 7
  • DOI: 10.1002/2017JG003825

Inorganic chemistry, gas compositions and dissolved organic carbon in fluids from sedimented young basaltic crust on the Juan de Fuca Ridge flanks
journal, May 2012


‘That which does not kill us only makes us stronger’: the role of carbon monoxide in thermophilic microbial consortia
journal, May 2009


Activity and phylogenetic diversity of sulfate-reducing microorganisms in low-temperature subsurface fluids within the upper oceanic crust
journal, January 2015

  • Robador, Alberto; Jungbluth, Sean P.; LaRowe, Douglas E.
  • Frontiers in Microbiology, Vol. 5
  • DOI: 10.3389/fmicb.2014.00748

The importance of designating type material for uncultured taxa
journal, January 2019

  • Chuvochina, Maria; Rinke, Christian; Parks, Donovan H.
  • Systematic and Applied Microbiology, Vol. 42, Issue 1
  • DOI: 10.1016/j.syapm.2018.07.003

Microbial diversity within basement fluids of the sediment-buried Juan de Fuca Ridge flank
journal, July 2012

  • Jungbluth, Sean P.; Grote, Jana; Lin, Huei-Ting
  • The ISME Journal, Vol. 7, Issue 1
  • DOI: 10.1038/ismej.2012.73

Hydrogen-limited growth of hyperthermophilic methanogens at deep-sea hydrothermal vents
journal, August 2012

  • Ver Eecke, H. C.; Butterfield, D. A.; Huber, J. A.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 34
  • DOI: 10.1073/pnas.1206632109

Isolation of Extremely Thermophilic Sulfate Reducers: Evidence for a Novel Branch of Archaebacteria
journal, May 1987


The physiology and habitat of the last universal common ancestor
journal, July 2016


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes
journal, May 2012


Energy yields from chemolithotrophic metabolisms in igneous basement of the Juan de Fuca ridge flank system
journal, January 2013


ARB: a software environment for sequence data
journal, February 2004


trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009


Binning metagenomic contigs by coverage and composition
journal, September 2014

  • Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino
  • Nature Methods, Vol. 11, Issue 11
  • DOI: 10.1038/nmeth.3103

Fluid and geochemical transport through oceanic crust: a transect across the eastern flank of the Juan de Fuca Ridge
journal, October 1999


Pathways and Bioenergetics of Anaerobic Carbon Monoxide Fermentation
journal, November 2015

  • Diender, Martijn; Stams, Alfons J. M.; Sousa, Diana Z.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01275

Life with Carbon Monoxide
journal, January 2004

  • Ragsdale, Stephen W.
  • Critical Reviews in Biochemistry and Molecular Biology, Vol. 39, Issue 3
  • DOI: 10.1080/10409230490496577

Big Data Paradigm: What is the Status of Privacy and Security?
journal, January 2017


Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

A new view of the tree of life
journal, April 2016


The origin of methanethiol in midocean ridge hydrothermal fluids
journal, March 2014

  • Reeves, E. P.; McDermott, J. M.; Seewald, J. S.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 15
  • DOI: 10.1073/pnas.1400643111

Genome Streamlining in a Cosmopolitan Oceanic Bacterium
journal, August 2005


dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication
journal, July 2017

  • Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon
  • The ISME Journal, Vol. 11, Issue 12
  • DOI: 10.1038/ismej.2017.126

Archaeoglobus fulgidus couples CO oxidation to sulfate reduction and acetogenesis with transient formate accumulation : The CO metabolism of
journal, April 2007


Thermodynamic limitations on microbially catalyzed reaction rates
journal, August 2012


The growing tree of Archaea: new perspectives on their diversity, evolution and ecology
journal, August 2017

  • Adam, Panagiotis S.; Borrel, Guillaume; Brochier-Armanet, Céline
  • The ISME Journal, Vol. 11, Issue 11
  • DOI: 10.1038/ismej.2017.122

Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle
journal, February 2018

  • Anantharaman, Karthik; Hausmann, Bela; Jungbluth, Sean P.
  • The ISME Journal, Vol. 12, Issue 7
  • DOI: 10.1038/s41396-018-0078-0

Methanogenesis and the Wood–Ljungdahl Pathway: An Ancient, Versatile, and Fragile Association
journal, May 2016

  • Borrel, Guillaume; Adam, Panagiotis S.; Gribaldo, Simonetta
  • Genome Biology and Evolution, Vol. 8, Issue 6
  • DOI: 10.1093/gbe/evw114

Complex archaea that bridge the gap between prokaryotes and eukaryotes
journal, May 2015

  • Spang, Anja; Saw, Jimmy H.; Jørgensen, Steffen L.
  • Nature, Vol. 521, Issue 7551
  • DOI: 10.1038/nature14447

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

Gene expression in the deep biosphere
journal, June 2013

  • Orsi, William D.; Edgcomb, Virginia P.; Christman, Glenn D.
  • Nature, Vol. 499, Issue 7457
  • DOI: 10.1038/nature12230

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

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

The two-domain tree of life is linked to a new root for the Archaea
journal, May 2015

  • Raymann, Kasie; Brochier-Armanet, Céline; Gribaldo, Simonetta
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 21
  • DOI: 10.1073/pnas.1420858112

Metabolic traits of an uncultured archaeal lineage -MSBL1- from brine pools of the Red Sea
journal, January 2016

  • Mwirichia, Romano; Alam, Intikhab; Rashid, Mamoon
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep19181

Mid-Ocean Ridge Hydrothermal Fluxes and the Chemical Composition of the Ocean
journal, May 1996


Microbial life under extreme energy limitation
journal, January 2013

  • Hoehler, Tori M.; Jørgensen, Bo Barker
  • Nature Reviews Microbiology, Vol. 11, Issue 2
  • DOI: 10.1038/nrmicro2939

Cytochromes c in Archaea: distribution, maturation, cell architecture, and the special case of Ignicoccus hospitalis
journal, May 2015


Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic complexes
journal, January 2018

  • Adam, Panagiotis S.; Borrel, Guillaume; Gribaldo, Simonetta
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 6
  • DOI: 10.1073/pnas.1716667115

Novel microbial assemblages inhabiting crustal fluids within mid-ocean ridge flank subsurface basalt
journal, February 2016

  • Jungbluth, Sean P.; Bowers, Robert M.; Lin, Huei-Ting
  • The ISME Journal, Vol. 10, Issue 8
  • DOI: 10.1038/ismej.2015.248

Enigmatic, ultrasmall, uncultivated Archaea
journal, April 2010

  • Baker, B. J.; Comolli, L. R.; Dick, G. J.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 19
  • DOI: 10.1073/pnas.0914470107

Archaeal biofilm formation
journal, August 2018

  • van Wolferen, Marleen; Orell, Alvaro; Albers, Sonja-Verena
  • Nature Reviews Microbiology, Vol. 16, Issue 11
  • DOI: 10.1038/s41579-018-0058-4