Phylogenetic and Functional Analysis of Metagenome Sequence from High-Temperature Archaeal Habitats Demonstrate Linkages between Metabolic Potential and Geochemistry

Inskeep, William P.; Jay, Zackary J.; Herrgard, Markus J.; Kozubal, Mark A.; Rusch, Douglas B.; Tringe, Susannah G.; Macur, Richard E.; Jennings, Ryan deM.; Boyd, Eric S.; Spear, John R.; Roberto, Francisco F.

doi:10.3389/fmicb.2013.00095

Phylogenetic and Functional Analysis of Metagenome Sequence from High-Temperature Archaeal Habitats Demonstrate Linkages between Metabolic Potential and Geochemistry

Journal Article · Tue Jan 01 00:00:00 EST 2013 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2013.00095· OSTI ID:1628087

Inskeep, William P. ^[1]; Jay, Zackary J. ^[2]; Herrgard, Markus J. ^[3]; Kozubal, Mark A. ^[2]; Rusch, Douglas B. ^[4]; Tringe, Susannah G. ^[5]; Macur, Richard E. ^[2]; Jennings, Ryan deM. ^[2]; Boyd, Eric S. ^[6]; Spear, John R. ^[7]; Roberto, Francisco F. ^[8]

Montana State Univ., Bozeman, MT (United States). Dept. of Land Resources and Environmental Sciences; Montana State Univ., Bozeman, MT (United States). Thermal Biology Inst.; DOE/OSTI
Montana State Univ., Bozeman, MT (United States). Dept. of Land Resources and Environmental Sciences
Technical Univ. of Denmark, Hørsholm (Denmark). Novo Nordisk Foundation Center for Biosustainability
Indiana Univ., Bloomington, IN (United States). Center for Genomics and Bioinformatics
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Montana State Univ., Bozeman, MT (United States). Thermal Biology Inst.; Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry
Colorado School of Mines, Golden, CO (United States). Dept. of Civil and Environmental Engineering
Newmont Mining Corporation, Englewood, CO (United States)

Geothermal habitats in Yellowstone National Park (YNP) provide an unparalleled opportunity to understand the environmental factors that control the distribution of archaea in thermal habitats. Here we describe, analyze, and synthesize metagenomic and geochemical data collected from seven high-temperature sites that contain microbial communities dominated by archaea relative to bacteria. The specific objectives of the study were to use metagenome sequencing to determine the structure and functional capacity of thermophilic archaeal-dominated microbial communities across a pH range from 2.5 to 6.4 and to discuss specific examples where the metabolic potential correlated with measured environmental parameters and geochemical processes occurring in situ. Random shotgun metagenome sequence (~40–45 Mb Sanger sequencing per site) was obtained from environmental DNA extracted from high-temperature sediments and/or microbial mats and subjected to numerous phylogenetic and functional analyses. Analysis of individual sequences (e.g., MEGAN and G + C content) and assemblies from each habitat type revealed the presence of dominant archaeal populations in all environments, 10 of whose genomes were largely reconstructed from the sequence data. Analysis of protein family occurrence, particularly of those involved in energy conservation, electron transport, and autotrophic metabolism, revealed significant differences in metabolic strategies across sites consistent with differences in major geochemical attributes (e.g., sulfide, oxygen, pH). These observations provide an ecological basis for understanding the distribution of indigenous archaeal lineages across high-temperature systems of YNP.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1628087

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 4; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Geomicrobiology of sublacustrine thermal vents in Yellowstone Lake: geochemical controls on microbial community structure and function Inskeep, William P.; Jay, Zackary J.; Macur, Richard E. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01044	journal	October 2015
Taxonomic and functional characteristics of microbial communities and their correlation with physicochemical properties of four geothermal springs in Odisha, India Badhai, Jhasketan; Ghosh, Tarini S.; Das, Subrata K. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01166	journal	October 2015
Microbial Community Structure of Activated Sludge in Treatment Plants with Different Wastewater Compositions Shchegolkova, Nataliya M.; Krasnov, George S.; Belova, Anastasia A. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00090	journal	February 2016
Metagenomics of Thermophiles with a Focus on Discovery of Novel Thermozymes DeCastro, María-Eugenia; Rodríguez-Belmonte, Esther; González-Siso, María-Isabel Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01521	journal	September 2016
Integration of Metagenomic and Stable Carbon Isotope Evidence Reveals the Extent and Mechanisms of Carbon Dioxide Fixation in High-Temperature Microbial Communities Jennings, Ryan de Montmollin; Moran, James J.; Jay, Zackary J. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00088	journal	February 2017
Sulfur Oxidation in the Acidophilic Autotrophic Acidithiobacillus spp. Wang, Rui; Lin, Jian-Qiang; Liu, Xiang-Mei Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03290	journal	January 2019
Global Microbiome Diversity Scaling in Hot Springs With DAR (Diversity-Area Relationship) Profiles Li, Lianwei; Ma, Zhanshan (Sam) Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00118	journal	February 2019
Pseudomonas PB1-Like Phages: Whole Genomes from Metagenomes Offer Insight into an Abundant Group of Bacteriophages Watkins, Siobhan; Sible, Emily; Putonti, Catherine Viruses, Vol. 10, Issue 6 https://doi.org/10.3390/v10060331	journal	June 2018
virMine: automated detection of viral sequences from complex metagenomic samples Garretto, Andrea; Hatzopoulos, Thomas; Putonti, Catherine PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6695	journal	January 2019
Occurrence and expression of novel methyl-coenzyme M reductase gene (mcrA) variants in hot spring sediments McKay, Luke J.; Hatzenpichler, Roland; Inskeep, William P. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-07354-x	journal	August 2017
Calditol-linked membrane lipids are required for acid tolerance in Sulfolobus acidocaldarius Zeng, Zhirui; Liu, Xiao-Lei; Wei, Jeremy H. Proceedings of the National Academy of Sciences, Vol. 115, Issue 51 https://doi.org/10.1073/pnas.1814048115	journal	December 2018
Microbial oxidative sulfur metabolism: biochemical evidence of the membrane-bound heterodisulfide reductase-like complex of the bacterium Aquifex aeolicus Boughanemi, Souhela; Lyonnet, Jordan; Infossi, Pascale FEMS Microbiology Letters, Vol. 363, Issue 15 https://doi.org/10.1093/femsle/fnw156	journal	June 2016
New archaeal viruses discovered by metagenomic analysis of viral communities in enrichment cultures Liu, Ying; Brandt, David; Ishino, Sonoko Environmental Microbiology, Vol. 21, Issue 6 https://doi.org/10.1111/1462-2920.14479	journal	January 2019
Multiscale analysis of autotroph-heterotroph interactions in a high-temperature microbial community Hunt, Kristopher A.; Jennings, Ryan M.; Inskeep, William P. PLOS Computational Biology, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pcbi.1006431	journal	September 2018

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