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 approximately 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.
authors.affiliation: Department of Earth and Planetary Science and Environmental Science, University of California, Berkeley, CA 94720, USA.
authors.forename: Brett J
authors.initials: BJ
authors.lastname: Baker
authors.forename: Luis R
authors.initials: LR
authors.lastname: Comolli
authors.forename: Gregory J
authors.initials: GJ
authors.lastname: Dick
authors.forename: Loren J
authors.initials: LJ
authors.lastname: Hauser
authors.forename: Doug
authors.initials: D
authors.lastname: Hyatt
authors.forename: Brian D
authors.initials: BD
authors.lastname: Dill
authors.forename: Miriam L
authors.initials: ML
authors.lastname: Land
authors.forename: Nathan C
authors.initials: NC
authors.lastname: Verberkmoes
authors.forename: Robert L
authors.initials: RL
authors.lastname: Hettich
authors.forename: Jillian F
authors.initials: JF
authors.lastname: Banfield
mesh_terms: D001105:Archaea / Q000166:cytology* / Q000235:genetics* / Q000378:metabolism / Q000648:ultrastructure; D019843:Archaeal Proteins / Q000145:classification / Q000235:genetics; D018441:Biofilms; D002453:Cell Cycle; D004261:DNA Replication; D020745:Genome, Archaeal / Q000235:genetics; D016680:Genome, Bacterial / Q000235:genetics; D008969:Molecular Sequence Data; D014176:Protein Biosynthesis; D040901:Proteomics; D013045:Species Specificity; D014158:Transcription, Genetic
chemical_list: D019843:Archaeal Proteins