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Title: Enigmatic, ultrasmall, uncultivated Archaea

Abstract

Metagenomics has provided access to genomes of as yet uncultivated microorganisms in natural environments, yet there are gaps in our knowledge particularly for Archaea that occur at relatively low abundance and in extreme environments. Ultrasmall cells (<500 nm in diameter) from lineages without cultivated representatives that branch near the crenarchaeal/euryarchaeal divide have been detected in a variety of acidic ecosystems. We reconstructed composite, near-complete 1-Mb genomes for three lineages, referred to as ARMAN (archaeal Richmond Mine acidophilic nanoorganisms), from environmental samples and a biofilm filtrate. Genes of two lineages are among the smallest yet described, enabling a 10% higher coding density than found genomes of the same size, and there are noncontiguous genes. No biological function could be inferred for up to 45% of genes and no more than 63% of the predicted proteins could be assigned to a revised set of archaeal clusters of orthologous groups. Some core metabolic genes are more common in Crenarchaeota than Euryarchaeota, up to 21% of genes have the highest sequence identity to bacterial genes, and 12 belong to clusters of orthologous groups that were previously exclusive to bacteria. A small subset of 3D cryo-electron tomographic reconstructions clearly show penetration of the ARMAN cellmore » wall and cytoplasmic membranes by protuberances extended from cells of the archaeal order Thermoplasmatales. Interspecies interactions, the presence of a unique internal tubular organelle [Comolli, et al. (2009) ISME J 3:159 167], and many genes previously only affiliated with Crenarchaea or Bacteria indicate extensive unique physiology in organisms that branched close to the time that Cren- and Euryarchaeotal lineages diverged.« less

Authors:
 [1];  [2];  [1];  [3];  [3];  [3];  [3];  [3];  [1]
  1. University of California, Berkeley
  2. Lawrence Berkeley National Laboratory (LBNL)
  3. ORNL
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1000730
DOE Contract Number:  
DE-AC05-00OR22725
Resource Type:
Journal Article
Journal Name:
Proceedings of the National Academy of Sciences
Additional Journal Information:
Journal Volume: 107; Journal Issue: 19; Journal ID: ISSN 0027--8424
Country of Publication:
United States
Language:
English

Citation Formats

Baker, Brett J., Comolli, Luis, Dick, Gregory J., Hauser, Loren John, Hyatt, Philip Douglas, Dill, Brian, Land, Miriam L, Verberkmoes, Nathan C, Hettich, Robert, and Banfield, Jillian F. Enigmatic, ultrasmall, uncultivated Archaea. United States: N. p., 2010. Web. doi:10.1073/pnas.0914470107.
Baker, Brett J., Comolli, Luis, Dick, Gregory J., Hauser, Loren John, Hyatt, Philip Douglas, Dill, Brian, Land, Miriam L, Verberkmoes, Nathan C, Hettich, Robert, & Banfield, Jillian F. Enigmatic, ultrasmall, uncultivated Archaea. United States. https://doi.org/10.1073/pnas.0914470107
Baker, Brett J., Comolli, Luis, Dick, Gregory J., Hauser, Loren John, Hyatt, Philip Douglas, Dill, Brian, Land, Miriam L, Verberkmoes, Nathan C, Hettich, Robert, and Banfield, Jillian F. Fri . "Enigmatic, ultrasmall, uncultivated Archaea". United States. https://doi.org/10.1073/pnas.0914470107.
@article{osti_1000730,
title = {Enigmatic, ultrasmall, uncultivated Archaea},
author = {Baker, Brett J. and Comolli, Luis and Dick, Gregory J. and Hauser, Loren John and Hyatt, Philip Douglas and Dill, Brian and Land, Miriam L and Verberkmoes, Nathan C and Hettich, Robert and Banfield, Jillian F.},
abstractNote = {Metagenomics has provided access to genomes of as yet uncultivated microorganisms in natural environments, yet there are gaps in our knowledge particularly for Archaea that occur at relatively low abundance and in extreme environments. Ultrasmall cells (<500 nm in diameter) from lineages without cultivated representatives that branch near the crenarchaeal/euryarchaeal divide have been detected in a variety of acidic ecosystems. We reconstructed composite, near-complete 1-Mb genomes for three lineages, referred to as ARMAN (archaeal Richmond Mine acidophilic nanoorganisms), from environmental samples and a biofilm filtrate. Genes of two lineages are among the smallest yet described, enabling a 10% higher coding density than found genomes of the same size, and there are noncontiguous genes. No biological function could be inferred for up to 45% of genes and no more than 63% of the predicted proteins could be assigned to a revised set of archaeal clusters of orthologous groups. Some core metabolic genes are more common in Crenarchaeota than Euryarchaeota, up to 21% of genes have the highest sequence identity to bacterial genes, and 12 belong to clusters of orthologous groups that were previously exclusive to bacteria. A small subset of 3D cryo-electron tomographic reconstructions clearly show penetration of the ARMAN cell wall and cytoplasmic membranes by protuberances extended from cells of the archaeal order Thermoplasmatales. Interspecies interactions, the presence of a unique internal tubular organelle [Comolli, et al. (2009) ISME J 3:159 167], and many genes previously only affiliated with Crenarchaea or Bacteria indicate extensive unique physiology in organisms that branched close to the time that Cren- and Euryarchaeotal lineages diverged.},
doi = {10.1073/pnas.0914470107},
url = {https://www.osti.gov/biblio/1000730}, journal = {Proceedings of the National Academy of Sciences},
issn = {0027--8424},
number = 19,
volume = 107,
place = {United States},
year = {2010},
month = {1}
}