skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Genomic Comparison of Two Family-Level Groups of the Uncultivated NAG1 Archaeal Lineage from Chemically and Geographically Disparate Hot Springs

Abstract

Recent progress based on single-cell genomics and metagenomic investigations of archaea in a variety of extreme environments has led to significant advances in our understanding of the diversity, evolution, and metabolic potential of archaea, yet the vast majority of archaeal diversity remains undersampled. In this work, we coordinated single-cell genomics with metagenomics in order to construct a near-complete genome from a deeply branching uncultivated archaeal lineage sampled from Great Boiling Spring (GBS) in the U.S. Great Basin, Nevada. This taxon is distantly related (distinct families) to an archaeal genome, designated “Novel Archaeal Group 1” (NAG1), which was extracted from a metagenome recovered from an acidic iron spring in Yellowstone National Park (YNP). We compared the metabolic predictions of the NAG1 lineage to better understand how these archaea could inhabit such chemically distinct environments. Similar to the NAG1 population previously studied in YNP, the NAG1 population from GBS is predicted to utilize proteins as a primary carbon source, ferment simple carbon sources, and use oxygen as a terminal electron acceptor under oxic conditions. However, GBS NAG1 populations contained distinct genes involved in central carbon metabolism and electron transfer, including nitrite reductase, which could confer the ability to reduce nitrite under anaerobicmore » conditions. Despite inhabiting chemically distinct environments with large variations in pH, GBS NAG1 populations shared many core genomic and metabolic features with the archaeon identified from YNP, yet were able to carve out a distinct niche at GBS.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [4];  [5]
  1. Northern Illinois Univ., DeKalb, IL (United States); Bigelow Lab. for Ocean Sciences, East Boothbay, ME (United States)
  2. California State Univ. (CalState), San Bernardino, CA (United States); Univ. of Nevada, Las Vegas, NV (United States)
  3. Univ. of Nevada, Las Vegas, NV (United States); Université Paris-Saclay, Jouy-en-Josas (France). Institut National de la Recherche Agronomique (INRA)
  4. Univ. of Nevada, Las Vegas, NV (United States)
  5. Northern Illinois Univ., DeKalb, IL (United States)
  6. Bigelow Lab. for Ocean Sciences, East Boothbay, ME (United States)
Publication Date:
Research Org.:
Nevada System of Higher Education (NSHE), Las Vegas, NV (United States); Univ. of California, Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE); USDOE Office of Science (SC)
OSTI Identifier:
1510510
Grant/Contract Number:  
EE0000716; AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; extreme microbiology; microbial ecology; uncultivated archaea; NAG1 lineage; Great Boiling Spring

Citation Formats

Becraft, Eric D., Dodsworth, Jeremy A., Murugapiran, Senthil K., Thomas, Scott C., Ohlsson, J. Ingemar, Stepanauskas, Ramunas, Hedlund, Brian P., and Swingley, Wesley D. Genomic Comparison of Two Family-Level Groups of the Uncultivated NAG1 Archaeal Lineage from Chemically and Geographically Disparate Hot Springs. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.02082.
Becraft, Eric D., Dodsworth, Jeremy A., Murugapiran, Senthil K., Thomas, Scott C., Ohlsson, J. Ingemar, Stepanauskas, Ramunas, Hedlund, Brian P., & Swingley, Wesley D. Genomic Comparison of Two Family-Level Groups of the Uncultivated NAG1 Archaeal Lineage from Chemically and Geographically Disparate Hot Springs. United States. https://doi.org/10.3389/fmicb.2017.02082
Becraft, Eric D., Dodsworth, Jeremy A., Murugapiran, Senthil K., Thomas, Scott C., Ohlsson, J. Ingemar, Stepanauskas, Ramunas, Hedlund, Brian P., and Swingley, Wesley D. Tue . "Genomic Comparison of Two Family-Level Groups of the Uncultivated NAG1 Archaeal Lineage from Chemically and Geographically Disparate Hot Springs". United States. https://doi.org/10.3389/fmicb.2017.02082. https://www.osti.gov/servlets/purl/1510510.
@article{osti_1510510,
title = {Genomic Comparison of Two Family-Level Groups of the Uncultivated NAG1 Archaeal Lineage from Chemically and Geographically Disparate Hot Springs},
author = {Becraft, Eric D. and Dodsworth, Jeremy A. and Murugapiran, Senthil K. and Thomas, Scott C. and Ohlsson, J. Ingemar and Stepanauskas, Ramunas and Hedlund, Brian P. and Swingley, Wesley D.},
abstractNote = {Recent progress based on single-cell genomics and metagenomic investigations of archaea in a variety of extreme environments has led to significant advances in our understanding of the diversity, evolution, and metabolic potential of archaea, yet the vast majority of archaeal diversity remains undersampled. In this work, we coordinated single-cell genomics with metagenomics in order to construct a near-complete genome from a deeply branching uncultivated archaeal lineage sampled from Great Boiling Spring (GBS) in the U.S. Great Basin, Nevada. This taxon is distantly related (distinct families) to an archaeal genome, designated “Novel Archaeal Group 1” (NAG1), which was extracted from a metagenome recovered from an acidic iron spring in Yellowstone National Park (YNP). We compared the metabolic predictions of the NAG1 lineage to better understand how these archaea could inhabit such chemically distinct environments. Similar to the NAG1 population previously studied in YNP, the NAG1 population from GBS is predicted to utilize proteins as a primary carbon source, ferment simple carbon sources, and use oxygen as a terminal electron acceptor under oxic conditions. However, GBS NAG1 populations contained distinct genes involved in central carbon metabolism and electron transfer, including nitrite reductase, which could confer the ability to reduce nitrite under anaerobic conditions. Despite inhabiting chemically distinct environments with large variations in pH, GBS NAG1 populations shared many core genomic and metabolic features with the archaeon identified from YNP, yet were able to carve out a distinct niche at GBS.},
doi = {10.3389/fmicb.2017.02082},
url = {https://www.osti.gov/biblio/1510510}, journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = ,
volume = 8,
place = {United States},
year = {2017},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 1 work
Citation information provided by
Web of Science

Figures / Tables:

Table 1 Table 1: NAG1 statistics for the Great Boiling Spring (GBS) single assembled genome (SAG) co-assembly, the GBS MLP metagenome assembly, and the Yellowstone National Park (YNP) metagenome assembly (Kozubal et al., 2013).

Save / Share:

Works referenced in this record:

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


Active-site remodelling in the bifunctional fructose-1,6-bisphosphate aldolase/phosphatase
journal, October 2011


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


The Binning of Metagenomic Contigs for Microbial Physiology of Mixed Cultures
journal, January 2012


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


Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park
journal, November 2012


CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats
journal, May 2007


Single-Cell-Genomics-Facilitated Read Binning of Candidate Phylum EM19 Genomes from Geothermal Spring Metagenomes
journal, December 2015


Evaluation of methods for extraction of bacteria from soil
journal, February 1995


BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences
journal, February 2016


Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences
journal, August 2014


Autotrophic carbon fixation in archaea
journal, May 2010


Distribution, diversity and ecology of aerobic CO-oxidizing bacteria
journal, February 2007


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


Alkaline pH homeostasis in bacteria: New insights
journal, November 2005


The RAST Server: Rapid Annotations using Subsystems Technology
journal, January 2008


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


Sediment microbial communities in Great Boiling Spring are controlled by temperature and distinct from water communities
journal, December 2012


The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012


Transaldolase of Methanocaldococcus jannaschii
journal, January 2004


Another Unusual Type of Citric Acid Cycle Enzyme in Helicobacter pylori: the Malate:Quinone Oxidoreductase
journal, June 2000


Microbiology and geochemistry of great boiling and mud hot springs in the United States Great Basin
journal, February 2009


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


Single-cell and metagenomic analyses indicate a fermentative and saccharolytic lifestyle for members of the OP9 lineage
journal, May 2013


Basic local alignment search tool
journal, October 1990


Accurate phylogenetic classification of variable-length DNA fragments
journal, December 2006


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


A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents
journal, July 2006


Cytochrome bd Oxidase, Oxidative Stress, and Dioxygen Tolerance of the Strictly Anaerobic Bacterium Moorella thermoacetica
journal, March 2005


Archaea in Symbioses
journal, January 2012


Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016


Genome sequence of the hyperthermophilic crenarchaeon Pyrobaculum aerophilum
journal, January 2002


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


‘Geoarchaeote NAG1’ is a deeply rooting lineage of the archaeal order Thermoproteales rather than a new phylum
journal, February 2014


Impact of single-cell genomics and metagenomics on the emerging view of extremophile “microbial dark matter”
journal, August 2014


MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0
journal, October 2013


Assembly and Succession of Iron Oxide Microbial Mat Communities in Acidic Geothermal Springs
journal, February 2016


DNA–DNA hybridization values and their relationship to whole-genome sequence similarities
journal, January 2007


CDD/SPARCLE: functional classification of proteins via subfamily domain architectures
journal, November 2016


    Works referencing / citing this record:

      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.