Enigmatic, ultrasmall, uncultivated Archaea.
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.
Baker
Brett J
BJ
Department of Earth and Planetary Science and Environmental Science, University of California, Berkeley, CA 94720, USA.
Comolli
Luis R
LR
Dick
Gregory J
GJ
Hauser
Loren J
LJ
Hyatt
Doug
D
Dill
Brian D
BD
Land
Miriam L
ML
Verberkmoes
Nathan C
NC
Hettich
Robert L
RL
Banfield
Jillian F
JF
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
D019843:Archaeal Proteins