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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 the Firmicutes phylum 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 “ Candidatus Desulforudis audaxviator” MP104C. While a limited number of differences were observed between the marine genome of “ Candidatus Desulfopertinax 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. Finally, 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 amore » natural means to investigate adaptations specific to 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)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1358388
Alternate Identifier(s):
OSTI ID: 1379633
Grant/Contract Number:
AC02-05CH11231
Resource Type:
Journal Article: 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. doi: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. doi: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 the Firmicutes phylum 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 “Candidatus Desulforudis audaxviator” MP104C. While a limited number of differences were observed between the marine genome of “Candidatus Desulfopertinax 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. Finally, 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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  • 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.more » 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.« less
  • Modern comparative genomics has been established, in part, by the sequencing and annotation of a broad range of microbial species. To gain further insights, new sequencing efforts are now dealing with the variety of strains or isolates that gives a species definition and range; however, this number vastly outstrips our ability to sequence them. Given the availability of a large number of microbial species, new whole genome approaches must be developed to fully leverage this information at the level of strain diversity that maximize discovery. Here, we describe how optical mapping, a single-molecule system, was used to identify and annotatemore » chromosomal alterations between bacterial strains represented by several species. Since whole-genome optical maps are ordered restriction maps, sequenced strains of Shigella flexneri serotype 2a (2457T and 301), Yersinia pestis (CO 92 and KIM), and Escherichia coli were aligned as maps to identify regions of homology and to further characterize them as possible insertions, deletions, inversions, or translocations. Importantly, an unsequenced Shigella flexneri strain (serotype Y strain AMC[328Y]) was optically mapped and aligned with two sequenced ones to reveal one novel locus implicated in serotype conversion and several other loci containing insertion sequence elements or phage-related gene insertions. Our results suggest that genomic rearrangements and chromosomal breakpoints are readily identified and annotated against a prototypic sequenced strain by using the tools of optical mapping.« less
  • The concept of a deep microbial biosphere has advanced over the past several decades from a hypothesis viewed with considerable skepticism to being widely accepted. Phylogenetically diverse prokaryotes have been cultured from or detected via characterization of directly-extracted nucleic acids from a wide range of deep terrestrial environments. Recent advances have linked the metabolic potential of these microorganisms, determined directly or inferred from phylogeny, to biogeochemical reactions determined via geochemical measurements and modeling. Buried organic matter or kerogen is an important source of energy for sustaining anaerobic heterotrophic microbial communities in deep sediments and sedimentary rock although rates of respirationmore » are among the slowest rates measured on the planet. In contrast, Subsurface Lithoautotrophic Microbial Ecosystems based on H2 as the primary energy source appear to dominate in many crystalline rock environments. These photosynthesis-independent ecosystems remain an enigma due to the difficulty in accessing and characterizing appropriate samples. Deep mines and dedicated rock laboratories, however, may offer unprecedented opportunities for investigating subsurface microbial communities and their interactions with the geosphere.« less
  • This study was aimed at understanding how the population structure of bacteria within terrestrial deep-subsurface environments correlates with the physical and chemical structure of their environment. Phylogenetic analysis was performed on strains of Arthrobacter collected from various depths. This included a number of different sedimentary units from the Yakima Barricade borehole at the U.S. Department of Energy's Hanford site, Washington, in August 1992. At the same time bacteria were isolated, detailed information on the physical, chemical, and microbiological characteristics of the sediments was collected. Phylogenetic trees were prepared from the 39 deep-subsurface Arthrobacter isolates (as well as 17 related typemore » strains) based on 16S rRNA and recA gene sequences. Analyses based on each gene independently were in general agreement. They showed that, for all but one of the strata (sedimentary layers characterized by their own unifying lithologic composition), the deep-subsurface isolates from the same stratum are largely monophyletic. Notably, the layers where this is true were composed of impermeable sediments. This suggests populations within each of these strata have remained isolated under constant, uniform conditions, selected for a particular dominant genotype in each stratum. Conversely, few strains isolated from a gravel-rich layer appeared along several lineages. This suggests that the higher-permeability gravel decreases the degree of isolation of this population (through greater groundwater flow), creating fluctuations in environmental conditions or allowing migration, such that a dominant population has not been established. No correlation was seen between the relationship of the strains and any particular chemical or physical characteristics of the sediments. This suggests that within sedimentary deep-subsurface environments, permeability of the deposits plays a major role in determining the genetic structure of resident bacterial populations.« less