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, 107 (19), 8806-11

Enigmatic, Ultrasmall, Uncultivated Archaea

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Enigmatic, Ultrasmall, Uncultivated Archaea

Brett J Baker et al. Proc Natl Acad Sci U S A.

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.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
The taxonomic affliations of the top blast hit for all proteins from each genome to the KEGG genome database. Crenarchaeota are shown on top and Euryarchaeota on the bottom of the diagram. The cutoff for the “no match” category was an e-value of 10−5.
Fig. 2.
Fig. 2.
Plot of archaeal and bacterial genomes (from National Center for Biotechnology Information database) sizes versus the number of protein encoding genes per genome.
Fig. 3.
Fig. 3.
A cryo-electron micrograph of the biofilm. Notice that the ARMAN cells are not connected to Thermoplasmatales cells present in this area. (Scale bar, 500 nm.)
Fig. 4.
Fig. 4.
Image illustrating interaction between ARMAN and a Thermoplasmatales lineage archaeon in the community. (A) A 1-pixel-thick slice through a cryo-electron tomographic reconstruction documenting interaction between an ARMAN cell on the right and a Thermoplasmatales lineage cell on the left. Also shown is the previously reported association of viruses and ARMAN cells (Upper and Lower, Right) and the presence of vacuoles in the single membrane-bounded Thermoplasmatales cell. A different slice through the reconstruction (2 pixels thick) shown in B illustrates the penetration of the ARMAN wall by the Thermoplasmatales cell. For a 3D movie of this field of view, see Movie S1. Also see Movie S2 and Movie S3 for other 3D examples of these connections. Ar, ARMAN; Tp, Thermoplasmatales lineage cell; Va, vacuole; VI, virus. (Scale bar in A, 300 nm; in B, 50 nm.)

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