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
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.
