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Title: Genomic comparisons of a bacterial lineage that inhabits both marine and terrestrial deep subsurface systems

Abstract

It is generally accepted that diverse, poorly characterized microorganisms reside deep within Earth’s crust. One such lineage of deep subsurface-dwelling bacteria is an uncultivated member of theFirmicutesphylum that can dominate molecular surveys from both marine and continental rock fracture fluids, sometimes forming the sole member of a single-species microbiome. Here, we reconstructed a genome from basalt-hosted fluids of the deep subseafloor along the eastern Juan de Fuca Ridge flank and used a phylogenomic analysis to show that, despite vast differences in geographic origin and habitat, it forms a monophyletic clade with the terrestrial deep subsurface genome of “CandidatusDesulforudis audaxviator” MP104C. While a limited number of differences were observed between the marine genome of “CandidatusDesulfopertinax cowenii” modA32 and its terrestrial relative that may be of potential adaptive importance, here it is revealed that the two are remarkably similar thermophiles possessing the genetic capacity for motility, sporulation, hydrogenotrophy, chemoorganotrophy, dissimilatory sulfate reduction, and the ability to fix inorganic carbon via the Wood-Ljungdahl pathway for chemoautotrophic growth. Our results provide insights into the genetic repertoire within marine and terrestrial members of a bacterial lineage that is widespread in the global deep subsurface biosphere, and provides a natural means to investigate adaptations specific tomore » these two environments.« less

Authors:
 [1];  [2];  [2];  [3];  [4]
  1. Univ. of Hawaii at Manoa, Honolulu, HI (United States); Univ. of Southern California, Los Angeles, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Bigelow Lab. for Ocean Sciences, East Boothbay, ME (United States)
  4. Univ. of Hawaii at Manoa, Kaneohe, HI (United States)
Publication Date:
Research Org.:
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1358388
Alternate Identifier(s):
OSTI ID: 1379633
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
PeerJ
Additional Journal Information:
Journal Volume: 5; Journal ID: ISSN 2167-8359
Publisher:
PeerJ Inc.
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; deep subsurface; microorganisms; Firmicutes; Juan de Fuca Ridge; chemoautotrophy; basement biosphere; sulfate reduction; sporulation; genomic; metagenomic

Citation Formats

Jungbluth, Sean P., Glavina del Rio, Tijana, Tringe, Susannah G., Stepanauskas, Ramunas, and Rappé, Michael S. Genomic comparisons of a bacterial lineage that inhabits both marine and terrestrial deep subsurface systems. United States: N. p., 2017. Web. doi:10.7717/peerj.3134.
Jungbluth, Sean P., Glavina del Rio, Tijana, Tringe, Susannah G., Stepanauskas, Ramunas, & Rappé, Michael S. Genomic comparisons of a bacterial lineage that inhabits both marine and terrestrial deep subsurface systems. United States. https://doi.org/10.7717/peerj.3134
Jungbluth, Sean P., Glavina del Rio, Tijana, Tringe, Susannah G., Stepanauskas, Ramunas, and Rappé, Michael S. Thu . "Genomic comparisons of a bacterial lineage that inhabits both marine and terrestrial deep subsurface systems". United States. https://doi.org/10.7717/peerj.3134. https://www.osti.gov/servlets/purl/1358388.
@article{osti_1358388,
title = {Genomic comparisons of a bacterial lineage that inhabits both marine and terrestrial deep subsurface systems},
author = {Jungbluth, Sean P. and Glavina del Rio, Tijana and Tringe, Susannah G. and Stepanauskas, Ramunas and Rappé, Michael S.},
abstractNote = {It is generally accepted that diverse, poorly characterized microorganisms reside deep within Earth’s crust. One such lineage of deep subsurface-dwelling bacteria is an uncultivated member of theFirmicutesphylum that can dominate molecular surveys from both marine and continental rock fracture fluids, sometimes forming the sole member of a single-species microbiome. Here, we reconstructed a genome from basalt-hosted fluids of the deep subseafloor along the eastern Juan de Fuca Ridge flank and used a phylogenomic analysis to show that, despite vast differences in geographic origin and habitat, it forms a monophyletic clade with the terrestrial deep subsurface genome of “CandidatusDesulforudis audaxviator” MP104C. While a limited number of differences were observed between the marine genome of “CandidatusDesulfopertinax cowenii” modA32 and its terrestrial relative that may be of potential adaptive importance, here it is revealed that the two are remarkably similar thermophiles possessing the genetic capacity for motility, sporulation, hydrogenotrophy, chemoorganotrophy, dissimilatory sulfate reduction, and the ability to fix inorganic carbon via the Wood-Ljungdahl pathway for chemoautotrophic growth. Our results provide insights into the genetic repertoire within marine and terrestrial members of a bacterial lineage that is widespread in the global deep subsurface biosphere, and provides a natural means to investigate adaptations specific to these two environments.},
doi = {10.7717/peerj.3134},
journal = {PeerJ},
number = ,
volume = 5,
place = {United States},
year = {Thu Apr 06 00:00:00 EDT 2017},
month = {Thu Apr 06 00:00:00 EDT 2017}
}

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Works referenced in this record:

IMG/M 4 version of the integrated metagenome comparative analysis system
journal, October 2013

  • Markowitz, Victor M.; Chen, I-Min A.; Chu, Ken
  • Nucleic Acids Research, Vol. 42, Issue D1, p. D568-D573
  • DOI: 10.1093/nar/gkt919

Fluids from Aging Ocean Crust That Support Microbial Life
journal, January 2003


Environmental Genomics Reveals a Single-Species Ecosystem Deep Within Earth
journal, October 2008


Characterization of bacterial diversity to a depth of 1500 m in the Outokumpu deep borehole, Fennoscandian Shield: Deep terrestrial biodiversity
journal, May 2011


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

Gene and translation initiation site prediction in metagenomic sequences
journal, July 2012


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


A metagenomic window into carbon metabolism at 3 km depth in Precambrian continental crust
journal, September 2015

  • Magnabosco, Cara; Ryan, Kathleen; Lau, Maggie C. Y.
  • The ISME Journal, Vol. 10, Issue 3
  • DOI: 10.1038/ismej.2015.150

Phylogenetic diversity of microorganisms in subseafloor crustal fluids from Holes 1025C and 1026B along the Juan de Fuca Ridge flank
journal, March 2014


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


EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data
journal, May 2011

  • Miller, Christopher S.; Baker, Brett J.; Thomas, Brian C.
  • Genome Biology, Vol. 12, Issue 5
  • DOI: 10.1186/gb-2011-12-5-r44

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


Advanced instrument system for real-time and time-series microbial geochemical sampling of the deep (basaltic) crustal biosphere
journal, March 2012

  • Cowen, James P.; Copson, David A.; Jolly, James
  • Deep Sea Research Part I: Oceanographic Research Papers, Vol. 61
  • DOI: 10.1016/j.dsr.2011.11.004

Dissolved organic carbon in ridge-axis and ridge-flank hydrothermal systems
journal, August 2006

  • Lang, Susan Q.; Butterfield, David A.; Lilley, Marvin D.
  • Geochimica et Cosmochimica Acta, Vol. 70, Issue 15
  • DOI: 10.1016/j.gca.2006.04.031

Long-Term Sustainability of a High-Energy, Low-Diversity Crustal Biome
journal, October 2006


IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011

  • Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1044

Easyfig: a genome comparison visualizer
journal, January 2011


Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes
journal, February 2009


RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006


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

Metagenome sequencing and 98 microbial genomes from Juan de Fuca Ridge flank subsurface fluids
journal, March 2017

  • Jungbluth, Sean P.; Amend, Jan P.; Rappé, Michael S.
  • Scientific Data, Vol. 4, Issue 1
  • DOI: 10.1038/sdata.2017.37

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


ProDeGe: a computational protocol for fully automated decontamination of genomes
journal, June 2015

  • Tennessen, Kristin; Andersen, Evan; Clingenpeel, Scott
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.100

MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm
journal, August 2014


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

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

Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016

  • Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw290

Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead
journal, October 2007

  • Konstantinidis, Konstantinos T.; Tiedje, James M.
  • Current Opinion in Microbiology, Vol. 10, Issue 5
  • DOI: 10.1016/j.mib.2007.08.006

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


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


SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012

  • Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 19, Issue 5
  • DOI: 10.1089/cmb.2012.0021

Accelerated Profile HMM Searches
journal, October 2011


The standard operating procedure of the DOE-JGI Metagenome Annotation Pipeline (MAP v.4)
journal, February 2016

  • Huntemann, Marcel; Ivanova, Natalia N.; Mavromatis, Konstantinos
  • Standards in Genomic Sciences, Vol. 11, Issue 1
  • DOI: 10.1186/s40793-016-0138-x

Towards a Genome-Based Taxonomy for Prokaryotes
journal, September 2005


Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population
journal, April 2015


Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

FR-HIT, a very fast program to recruit metagenomic reads to homologous reference genomes
journal, April 2011


A Rapid Bootstrap Algorithm for the RAxML Web Servers
journal, October 2008

  • Stamatakis, Alexandros; Hoover, Paul; Rougemont, Jacques
  • Systematic Biology, Vol. 57, Issue 5
  • DOI: 10.1080/10635150802429642

PhyloSift: phylogenetic analysis of genomes and metagenomes
journal, January 2014

  • Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.243

Variations in microbial carbon sources and cycling in the deep continental subsurface
journal, January 2016

  • Simkus, Danielle N.; Slater, Greg F.; Lollar, Barbara Sherwood
  • Geochimica et Cosmochimica Acta, Vol. 173
  • DOI: 10.1016/j.gca.2015.10.003

pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree
journal, October 2010

  • Matsen, Frederick A.; Kodner, Robin B.; Armbrust, E. Virginia
  • BMC Bioinformatics, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2105-11-538

Genomic insights that advance the species definition for prokaryotes
journal, February 2005

  • Konstantinidis, K. T.; Tiedje, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 7
  • DOI: 10.1073/pnas.0409727102

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

jModelTest 2: more models, new heuristics and parallel computing
journal, July 2012

  • Darriba, Diego; Taboada, Guillermo L.; Doallo, Ramón
  • Nature Methods, Vol. 9, Issue 8
  • DOI: 10.1038/nmeth.2109

PhyloSift: Phylogenetic analysis of genomes and metagenomes
dataset, January 2013


PhyloSift: Phylogenetic analysis of genomes and metagenomes
dataset, January 2013


Salinimonas marina sp. nov. Isolated from Jeju Island Marine Sediment
journal, June 2021


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


Dissolved organic carbon in ridge-axis and ridge-flank hydrothermal systems
journal, August 2006

  • Lang, Susan Q.; Butterfield, David A.; Lilley, Marvin D.
  • Geochimica et Cosmochimica Acta, Vol. 70, Issue 15
  • DOI: 10.1016/j.gca.2006.04.031

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


Variations in microbial carbon sources and cycling in the deep continental subsurface
journal, January 2016

  • Simkus, Danielle N.; Slater, Greg F.; Lollar, Barbara Sherwood
  • Geochimica et Cosmochimica Acta, Vol. 173
  • DOI: 10.1016/j.gca.2015.10.003

Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead
journal, October 2007

  • Konstantinidis, Konstantinos T.; Tiedje, James M.
  • Current Opinion in Microbiology, Vol. 10, Issue 5
  • DOI: 10.1016/j.mib.2007.08.006

Formation of Ammonium from Nitrate During Chemolithoautotrophic Growth of the Extremely Thermophilic Bacterium Ammonifex degensii gen. nov. sp. nov.
journal, March 1996


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

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

Genetic basis for the establishment of endosymbiosis in Paramecium
journal, January 2019


Anaerobic hydrocarbon degradation in candidate phylum ‘Atribacteria’ (JS1) inferred from genomics
journal, June 2019


Rhizosphere bacteriome structure and functions
journal, February 2022


Characterizing the molecular regulation of inhibitory immune checkpoints with multimodal single-cell screens
journal, March 2021


Microevolution of Campylobacter jejuni during long-term infection in an immunocompromised host
journal, June 2020


Metagenome sequencing and 98 microbial genomes from Juan de Fuca Ridge flank subsurface fluids
journal, March 2017

  • Jungbluth, Sean P.; Amend, Jan P.; Rappé, Michael S.
  • Scientific Data, Vol. 4, Issue 1
  • DOI: 10.1038/sdata.2017.37

A Rapid Bootstrap Algorithm for the RAxML Web Servers
journal, October 2008

  • Stamatakis, Alexandros; Hoover, Paul; Rougemont, Jacques
  • Systematic Biology, Vol. 57, Issue 5
  • DOI: 10.1080/10635150802429642

Easyfig: a genome comparison visualizer
journal, January 2011


FR-HIT, a very fast program to recruit metagenomic reads to homologous reference genomes
journal, April 2011


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


Gene and translation initiation site prediction in metagenomic sequences
journal, July 2012


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


IMG/M 4 version of the integrated metagenome comparative analysis system
journal, October 2013

  • Markowitz, Victor M.; Chen, I-Min A.; Chu, Ken
  • Nucleic Acids Research, Vol. 42, Issue D1, p. D568-D573
  • DOI: 10.1093/nar/gkt919

Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes
journal, February 2009


Fluids from Aging Ocean Crust That Support Microbial Life
journal, January 2003


Long-Term Sustainability of a High-Energy, Low-Diversity Crustal Biome
journal, October 2006


Updating Prokaryotic Taxonomy
journal, September 2005


MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm
journal, August 2014


EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data
journal, May 2011

  • Miller, Christopher S.; Baker, Brett J.; Thomas, Brian C.
  • Genome Biology, Vol. 12, Issue 5
  • DOI: 10.1186/gb-2011-12-5-r44

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

Accelerated Profile HMM Searches
journal, October 2011


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


ProDeGe: a computational protocol for fully automated decontamination of genomes
text, January 2016

  • James, Han,; L., Dangl, Jeff; Scott, Clingenpeel,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/xvw7-9p10

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

Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population
journal, April 2015


pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree
preprint, January 2010


PhyloSift: phylogenetic analysis of genomes and metagenomes
journal, January 2014

  • Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.243

Works referencing / citing this record:

Ecology of Subseafloor Crustal Biofilms
journal, August 2019

  • Ramírez, Gustavo A.; Garber, Arkadiy I.; Lecoeuvre, Aurélien
  • Frontiers in Microbiology, Vol. 10
  • DOI: 10.3389/fmicb.2019.01983

Domestication of previously uncultivated Candidatus Desulforudis audaxviator from a deep aquifer in Siberia sheds light on its physiology and evolution
journal, March 2019

  • Karnachuk, Olga V.; Frank, Yulia A.; Lukina, Anastasia P.
  • The ISME Journal, Vol. 13, Issue 8
  • DOI: 10.1038/s41396-019-0402-3

A metagenomic window into the 2-km-deep terrestrial subsurface aquifer revealed multiple pathways of organic matter decomposition
journal, August 2018

  • Kadnikov, Vitaly V.; Mardanov, Andrey V.; Beletsky, Alexey V.
  • FEMS Microbiology Ecology, Vol. 94, Issue 10
  • DOI: 10.1093/femsec/fiy152

Energy and carbon metabolisms in a deep terrestrial subsurface fluid microbial community
journal, June 2017

  • Momper, Lily; Jungbluth, Sean P.; Lee, Michael D.
  • The ISME Journal, Vol. 11, Issue 10
  • DOI: 10.1038/ismej.2017.94

Ecology of Subseafloor Crustal Biofilms
journal, August 2019

  • Ramírez, Gustavo A.; Garber, Arkadiy I.; Lecoeuvre, Aurélien
  • Frontiers in Microbiology, Vol. 10
  • DOI: 10.3389/fmicb.2019.01983