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Title: Ecophysiology of an uncultivated lineage of Aigarchaeota from an oxic, hot spring filamentous ‘streamer’ community

Abstract

In this study, the candidate archaeal phylum ‘Aigarchaeota’ contains microorganisms from terrestrial and subsurface geothermal ecosystems. The phylogeny and metabolic potential of Aigarchaeota has been deduced from several recent single-cell amplified genomes; however, a detailed description of their metabolic potential and in situ transcriptional activity is absent. Here, we report a comprehensive metatranscriptome-based reconstruction of the in situ metabolism of Aigarchaeota in an oxic, hot spring filamentous ‘streamer’ community. Fluorescence in situ hybridization showed that these newly discovered Aigarchaeota are filamentous, which is consistent with the presence and transcription of an actin-encoding gene. Aigarchaeota filaments are intricately associated with other community members, which include both bacteria (for example, filamentous Thermocrinis spp.) and archaea. Metabolic reconstruction of genomic and metatranscriptomic data suggests that this aigarchaeon is an aerobic, chemoorganoheterotroph with autotrophic potential. A heme copper oxidase complex was identified in the environmental genome assembly and highly transcribed in situ. Potential electron donors include acetate, fatty acids, amino acids, sugars and aromatic compounds, which may originate from extracellular polymeric substances produced by other microorganisms shown to exist in close proximity and/or autochthonous dissolved organic carbon (OC). Transcripts related to genes specific to each of these potential electron donors were identified, indicating thatmore » this aigarchaeon likely utilizes several OC substrates. Characterized members of this lineage cannot synthesize heme, and other cofactors and vitamins de novo, which suggests auxotrophy. We propose the name Candidatus ‘Calditenuis aerorheumensis’ for this aigarchaeon, which describes its filamentous morphology and its primary electron acceptor, oxygen.« less

Authors:
 [1];  [1];  [2];  [3];  [4];  [1];  [5]; ORCiD logo [6]; ORCiD logo [2];  [7]
  1. Montana State Univ., Bozeman, MT (United States)
  2. Univ. of Vienna, Vienna (Austria)
  3. Indiana Univ., Bloomington, IN (United States)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  5. Montana State Univ., Bozeman, MT (United States); Sustainable Bioproducts LLC, Bozeman, MT (United States)
  6. Dept. of Energy-Joint Genome Institute, Walnut Creek, CA (United States)
  7. Montana State Univ., Bozeman, MT (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1249370
Report Number(s):
PNNL-SA-108271
Journal ID: ISSN 1751-7362; ismej201583
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Beam, Jacob P., Jay, Zackary J., Schmid, Markus C., Rusch, Douglas B., Romine, Margaret F., Jennings, Ryan de M., Kozubal, Mark A., Tringe, Susannah G., Wagner, Michael, and Inskeep, William P. Ecophysiology of an uncultivated lineage of Aigarchaeota from an oxic, hot spring filamentous ‘streamer’ community. United States: N. p., 2015. Web. doi:10.1038/ismej.2015.83.
Beam, Jacob P., Jay, Zackary J., Schmid, Markus C., Rusch, Douglas B., Romine, Margaret F., Jennings, Ryan de M., Kozubal, Mark A., Tringe, Susannah G., Wagner, Michael, & Inskeep, William P. Ecophysiology of an uncultivated lineage of Aigarchaeota from an oxic, hot spring filamentous ‘streamer’ community. United States. doi:10.1038/ismej.2015.83.
Beam, Jacob P., Jay, Zackary J., Schmid, Markus C., Rusch, Douglas B., Romine, Margaret F., Jennings, Ryan de M., Kozubal, Mark A., Tringe, Susannah G., Wagner, Michael, and Inskeep, William P. Fri . "Ecophysiology of an uncultivated lineage of Aigarchaeota from an oxic, hot spring filamentous ‘streamer’ community". United States. doi:10.1038/ismej.2015.83. https://www.osti.gov/servlets/purl/1249370.
@article{osti_1249370,
title = {Ecophysiology of an uncultivated lineage of Aigarchaeota from an oxic, hot spring filamentous ‘streamer’ community},
author = {Beam, Jacob P. and Jay, Zackary J. and Schmid, Markus C. and Rusch, Douglas B. and Romine, Margaret F. and Jennings, Ryan de M. and Kozubal, Mark A. and Tringe, Susannah G. and Wagner, Michael and Inskeep, William P.},
abstractNote = {In this study, the candidate archaeal phylum ‘Aigarchaeota’ contains microorganisms from terrestrial and subsurface geothermal ecosystems. The phylogeny and metabolic potential of Aigarchaeota has been deduced from several recent single-cell amplified genomes; however, a detailed description of their metabolic potential and in situ transcriptional activity is absent. Here, we report a comprehensive metatranscriptome-based reconstruction of the in situ metabolism of Aigarchaeota in an oxic, hot spring filamentous ‘streamer’ community. Fluorescence in situ hybridization showed that these newly discovered Aigarchaeota are filamentous, which is consistent with the presence and transcription of an actin-encoding gene. Aigarchaeota filaments are intricately associated with other community members, which include both bacteria (for example, filamentous Thermocrinis spp.) and archaea. Metabolic reconstruction of genomic and metatranscriptomic data suggests that this aigarchaeon is an aerobic, chemoorganoheterotroph with autotrophic potential. A heme copper oxidase complex was identified in the environmental genome assembly and highly transcribed in situ. Potential electron donors include acetate, fatty acids, amino acids, sugars and aromatic compounds, which may originate from extracellular polymeric substances produced by other microorganisms shown to exist in close proximity and/or autochthonous dissolved organic carbon (OC). Transcripts related to genes specific to each of these potential electron donors were identified, indicating that this aigarchaeon likely utilizes several OC substrates. Characterized members of this lineage cannot synthesize heme, and other cofactors and vitamins de novo, which suggests auxotrophy. We propose the name Candidatus ‘Calditenuis aerorheumensis’ for this aigarchaeon, which describes its filamentous morphology and its primary electron acceptor, oxygen.},
doi = {10.1038/ismej.2015.83},
journal = {The ISME Journal},
number = 1,
volume = 10,
place = {United States},
year = {2015},
month = {7}
}

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