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

Title: 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.
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.

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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, Vol. 4; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Physiology, Metabolism, and Fossilization of Hot-Spring Filamentous Microbial Mats Dong, Yiran; Sanford, Robert A.; Inskeep, William P. Astrobiology, Vol. 19, Issue 12 https://doi.org/10.1089/ast.2018.1965	journal	December 2019
Merging metagenomics and geochemistry reveals environmental controls on biological diversity and evolution Alsop, Eric B.; Boyd, Eric S.; Raymond, Jason BMC Ecology, Vol. 14, Issue 1 https://doi.org/10.1186/1472-6785-14-16	journal	May 2014
The distribution, diversity, and importance of 16S rRNA gene introns in the order Thermoproteales Jay, Zackary J.; Inskeep, William P. Biology Direct, Vol. 10, Issue 1 https://doi.org/10.1186/s13062-015-0065-6	journal	July 2015
Microbial Community Structure and Arsenic Biogeochemistry in an Acid Vapor-Formed Spring in Tengchong Geothermal Area, China Jiang, Zhou; Li, Ping; Jiang, Dawei PLOS ONE, Vol. 11, Issue 1 https://doi.org/10.1371/journal.pone.0146331	journal	January 2016
Hydrogen Peroxide Cycling in High-Temperature Acidic Geothermal Springs and Potential Implications for Oxidative Stress Response Meslé, Margaux M.; Beam, Jacob P.; Jay, Zackary J. Frontiers in Marine Science, Vol. 4 https://doi.org/10.3389/fmars.2017.00130	journal	May 2017
The YNP metagenome project: environmental parameters responsible for microbial distribution in the Yellowstone geothermal ecosystem Inskeep, William Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00067	journal	January 2013
Phylogeny and phylogeography of functional genes shared among seven terrestrial subsurface metagenomes reveal N-cycling and microbial evolutionary relationships Lau, Maggie C. Y.; Cameron, Connor; Magnabosco, Cara Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00531	journal	October 2014
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
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
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

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