Integration of metagenomic and stable carbon isotope evidence reveals the extent and mechanisms of carbon dioxide fixation in high-temperature microbial communities
Abstract
Biological fixation of CO2 is the primary mechanism of C reduction in natural systems, and provides a diverse suite of organic compounds utilized by chemoorganoheterotrophs. The extent and mechanisms of CO2 fixation were evaluated across a comprehensive set of high-temperature, chemotrophic microbial communities in Yellowstone National Park by combining metagenomic and stable 13C isotope analyses. Fifteen geothermal sites representing three distinct habitat types (iron-oxide mats, anoxic sulfur sediments, and filamentous ‘streamer’ communities) were investigated. Genes of the 3-hydroxypropionate/4-hydroxybutyrate, dicarboxylate/4-hydroxybutyrate, and reverse tricarboxylic acid CO2 fixation pathways were identified in assembled genome sequence corresponding to the predominant Crenarchaeota and Aquificales observed across this habitat range. Stable 13C analyses of dissolved inorganic and organic C (DIC, DOC), and possible landscape C sources were used to interpret the 13C content of microbial community samples. Isotope mixing models showed that the minimum amounts of autotrophic C in microbial biomass were > 50 % in the majority of communities analyzed, but were also dependent on the amounts of heterotrophy and/or accumulation of landscape C. Furthermore, the significance of CO2 as a C source in these communities provides a foundation for understanding metabolic linkages among autotrophs and heterotrophs, community assembly and succession, and the likely coevolutionmore »
- Authors:
-
- Montana State Univ., Bozeman, MT (United States); Mercer Univ., Macon, GA (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Montana State Univ., Bozeman, MT (United States)
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1339794
- Report Number(s):
- PNNL-SA-119791
Journal ID: ISSN 1664-302X; KP1601010
- Grant/Contract Number:
- AC05-76RL01830
- Resource Type:
- 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; autotrophy; CO2 fixation; stable C isotopes; geothermal; Aquificales; Crenarchaeota
Citation Formats
Jennings, Ryan de Montmollin, Moran, James J., Jay, Zackary J., Beam, Jacob P., Whitmore, Laura M., Kozubal, Mark A., Kreuzer, Helen W., and Inskeep, William P. Integration of metagenomic and stable carbon isotope evidence reveals the extent and mechanisms of carbon dioxide fixation in high-temperature microbial communities. United States: N. p., 2017.
Web. doi:10.3389/fmicb.2017.00088.
Jennings, Ryan de Montmollin, Moran, James J., Jay, Zackary J., Beam, Jacob P., Whitmore, Laura M., Kozubal, Mark A., Kreuzer, Helen W., & Inskeep, William P. Integration of metagenomic and stable carbon isotope evidence reveals the extent and mechanisms of carbon dioxide fixation in high-temperature microbial communities. United States. https://doi.org/10.3389/fmicb.2017.00088
Jennings, Ryan de Montmollin, Moran, James J., Jay, Zackary J., Beam, Jacob P., Whitmore, Laura M., Kozubal, Mark A., Kreuzer, Helen W., and Inskeep, William P. Fri .
"Integration of metagenomic and stable carbon isotope evidence reveals the extent and mechanisms of carbon dioxide fixation in high-temperature microbial communities". United States. https://doi.org/10.3389/fmicb.2017.00088. https://www.osti.gov/servlets/purl/1339794.
@article{osti_1339794,
title = {Integration of metagenomic and stable carbon isotope evidence reveals the extent and mechanisms of carbon dioxide fixation in high-temperature microbial communities},
author = {Jennings, Ryan de Montmollin and Moran, James J. and Jay, Zackary J. and Beam, Jacob P. and Whitmore, Laura M. and Kozubal, Mark A. and Kreuzer, Helen W. and Inskeep, William P.},
abstractNote = {Biological fixation of CO2 is the primary mechanism of C reduction in natural systems, and provides a diverse suite of organic compounds utilized by chemoorganoheterotrophs. The extent and mechanisms of CO2 fixation were evaluated across a comprehensive set of high-temperature, chemotrophic microbial communities in Yellowstone National Park by combining metagenomic and stable 13C isotope analyses. Fifteen geothermal sites representing three distinct habitat types (iron-oxide mats, anoxic sulfur sediments, and filamentous ‘streamer’ communities) were investigated. Genes of the 3-hydroxypropionate/4-hydroxybutyrate, dicarboxylate/4-hydroxybutyrate, and reverse tricarboxylic acid CO2 fixation pathways were identified in assembled genome sequence corresponding to the predominant Crenarchaeota and Aquificales observed across this habitat range. Stable 13C analyses of dissolved inorganic and organic C (DIC, DOC), and possible landscape C sources were used to interpret the 13C content of microbial community samples. Isotope mixing models showed that the minimum amounts of autotrophic C in microbial biomass were > 50 % in the majority of communities analyzed, but were also dependent on the amounts of heterotrophy and/or accumulation of landscape C. Furthermore, the significance of CO2 as a C source in these communities provides a foundation for understanding metabolic linkages among autotrophs and heterotrophs, community assembly and succession, and the likely coevolution of deeply-branching thermophiles.},
doi = {10.3389/fmicb.2017.00088},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {Fri Feb 03 00:00:00 EST 2017},
month = {Fri Feb 03 00:00:00 EST 2017}
}
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Ecophysiology of an uncultivated lineage of Aigarchaeota from an oxic, hot spring filamentous ‘streamer’ community
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- Annual Review of Ecology and Systematics, Vol. 18, Issue 1
Evolutionary and Ecological Aspects of Photosynthetic Pathway Variation
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Old Acetogens, New Light
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Metagenomes from High-Temperature Chemotrophic Systems Reveal Geochemical Controls on Microbial Community Structure and Function
journal, March 2010
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- PLoS ONE, Vol. 5, Issue 3
The YNP metagenome project: environmental parameters responsible for microbial distribution in the Yellowstone geothermal ecosystem
journal, January 2013
- Inskeep, William
- Frontiers in Microbiology, Vol. 4
Metagenome Sequence Analysis of Filamentous Microbial Communities Obtained from Geochemically Distinct Geothermal Channels Reveals Specialization of Three Aquificales Lineages
journal, January 2013
- Takacs-Vesbach, Cristina; Inskeep, William P.; Jay, Zackary J.
- Frontiers in Microbiology, Vol. 4
Phylogenetic and Functional Analysis of Metagenome Sequence from High-Temperature Archaeal Habitats Demonstrate Linkages between Metabolic Potential and Geochemistry
journal, January 2013
- Inskeep, William P.; Jay, Zackary J.; Herrgard, Markus J.
- Frontiers in Microbiology, Vol. 4
Assembly and Succession of Iron Oxide Microbial Mat Communities in Acidic Geothermal Springs
journal, February 2016
- Beam, Jacob P.; Bernstein, Hans C.; Jay, Zackary J.
- Frontiers in Microbiology, Vol. 7
Novel, Deep-Branching Heterotrophic Bacterial Populations Recovered from Thermal Spring Metagenomes
journal, March 2016
- Colman, Daniel R.; Jay, Zackary J.; Inskeep, William P.
- Frontiers in Microbiology, Vol. 7
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- PLOS Computational Biology, Vol. 14, Issue 9
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- Schuler, Caleb G.; Havig, Jeff R.; Hamilton, Trinity L.
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Occurrence and expression of novel methyl-coenzyme M reductase gene (mcrA) variants in hot spring sediments
journal, August 2017
- McKay, Luke J.; Hatzenpichler, Roland; Inskeep, William P.
- Scientific Reports, Vol. 7, Issue 1
Multiscale analysis of autotroph-heterotroph interactions in a high-temperature microbial community
journal, September 2018
- Hunt, Kristopher A.; Jennings, Ryan M.; Inskeep, William P.
- PLOS Computational Biology, Vol. 14, Issue 9
Position-Specific Metabolic Probing and Metagenomics of Microbial Communities Reveal Conserved Central Carbon Metabolic Network Activities at High Temperatures
journal, July 2019
- Thomas, Scott C.; Tamadonfar, Kevin O.; Seymour, Cale O.
- Frontiers in Microbiology, Vol. 10