The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism

Abstract

The hyperthermophile Nanoarchaeum equitans is an obligate symbiont growing in coculture with the crenarchaeon Ignicoccus. Ribosomal protein and rRNA-based phylogenies place its branching point early in the archaeal lineage, representing the new archaeal kingdom Nanoarchaeota. The N. equitans genome (490,885 base pairs) encodes the machinery for information processing and repair, but lacks genes for lipid, cofactor, amino acid, or nucleotide biosyntheses. It is the smallest microbial genome sequenced to date, and also one of the most compact, with 95% of the DNA predicted to encode proteins or stable RNAs. Its limited biosynthetic and catabolic capacity indicates that N. equitans' symbiotic relationship to Ignicoccus is parasitic, making it the only known archaeal parasite. Unlike the small genomes of bacterial parasites that are undergoing reductive evolution, N. equitans has few pseudogenes or extensive regions of noncoding DNA. This organism represents a basal archaeal lineage and has a highly reduced genome.

Fig. 2.

Alanylation of unfractionated M. jannaschii tRNA by alanyl–tRNA synthetases. The purification and aminoacylation procedures were adapted from Ahel et al. (22) and are detailed in Materials and Methods. The enzymes used are M. jannaschii AlaRS (filled squares), N. equitans AlaRS1 N-terminal part (open circles), N. equitans AlaRS2 C-terminal part (filled triangles), and N. equitans AlaRS1 + AlaRS2 (filled circles).

Fig. 1.

Correlation between microbial genome size and the number of predicted coding DNA sequences CDS. Bacterial genomes predicted to be undergoing reductive evolution are indicated by open circles, whereas other genomes are indicated by filled circles. The N. equitans genome is marked by “x”.(Inset) An expansion of the data from small microbial genomes with the abscissa shown in genome size units of kbp.

Fig. 3.

Phylogenetic position of N. equitans within the Archaea. The tree was determined by the maximum likelihood method, based on 35 concatenated ribosomal protein sequences. Numbers indicate percentage of bootstrap resamplings. The scale bar corresponds to 10 estimated substitutions per 100 amino acid positions.