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Title: 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 CO 2 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 CO 2 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 CO 2 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 CO 2 as a C source in these communities provides a foundation for understanding metabolic linkages among autotrophs and heterotrophs, community assembly and succession,more » and the likely coevolution of deeply-branching thermophiles.« less

Authors:
 [1];  [2];  [3];  [1];  [2];  [3];  [2];  [3]
  1. Montana State Univ., Bozeman, MT (United States); Mercer Univ., Macon, GA (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. Montana State Univ., Bozeman, MT (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (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:
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; 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. 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., 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. doi: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},
issn = {1664-302X},
number = ,
volume = 8,
place = {United States},
year = {2017},
month = {2}
}

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    Hot Spring Microbial Community Composition, Morphology, and Carbon Fixation: Implications for Interpreting the Ancient Rock Record
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