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

Journal Article · · The ISME Journal
 [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)
+ Show Author Affiliations

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.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC05-76RL01830
OSTI ID:
1249370
Report Number(s):
PNNL-SA-108271; ismej201583
Journal Information:
The ISME Journal, Vol. 10, Issue 1; ISSN 1751-7362
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 30 works
Citation information provided by
Web of Science

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Cited By (26)

Novel, Deep-Branching Heterotrophic Bacterial Populations Recovered from Thermal Spring Metagenomes journal March 2016
Phylogenomics suggests oxygen availability as a driving force in Thaumarchaeota evolution journal April 2019
Position-Specific Metabolic Probing and Metagenomics of Microbial Communities Reveal Conserved Central Carbon Metabolic Network Activities at High Temperatures journal July 2019
The growing tree of Archaea: new perspectives on their diversity, evolution and ecology journal August 2017
Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota journal July 2018
The deep, hot biosphere: Twenty-five years of retrospection journal July 2017
Name Abstract for Calditenuis aerorheumatis dataset January 2016
Name Abstract for Calditenuis dataset January 2016
Nomenclature Abstract for Calditenuis aerorheumensis (sic) Beam et al. 2016. dataset January 2016
Nomenclature Abstract for Incertae sedis 379 Beam et al. 2016. dataset January 2019
Nomenclature Abstract for Aigarchaeota Beam et al. 2016. dataset January 2019
Nomenclature Abstract for Incertae sedis 378 Beam et al. 2016. dataset January 2019
Exemplar Abstract for Calditenuis aerorheumensis (sic) Beam et al. 2016 and Calditenuis aerorheumatis corrig. Beam et al. 2016. dataset January 2019
Comparative Analysis of Microbial Diversity Across Temperature Gradients in Hot Springs From Yellowstone and Iceland journal July 2020
Taxonomic Abstract for the order Incertae sedis 379 dataset January 2016
Evaluation of 16S rRNA Gene Primer Pairs for Monitoring Microbial Community Structures Showed High Reproducibility within and Low Comparability between Datasets Generated with Multiple Archaeal and Bacterial Primer Pairs journal August 2016
Geochemical and Metagenomic Characterization of Jinata Onsen, a Proterozoic-Analog Hot Spring, Reveals Novel Microbial Diversity including Iron-Tolerant Phototrophs and Thermophilic Lithotrophs journal January 2019
Two distinct pools of B 12 analogs reveal community interdependencies in the ocean journal December 2016
Metatranscriptomic and comparative genomic insights into resuscitation mechanisms during enrichment culturing journal December 2018
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Taxonomic Abstract for the genus Calditenuis dataset January 2016
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Taxon Abstract for the family Incertae sedis 380 dataset January 2016

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