Ribosomal Protein Cluster Organization in Asgard Archaea.

Abstract

It has been proposed that the superphylum of Asgard Archaea may represent a historical link between the Archaea and Eukarya. Following the discovery of the Archaea, it was soon appreciated that archaeal ribosomes were more similar to those of Eukarya rather than Bacteria. Coupled with other eukaryotic-like features, it has been suggested that the Asgard Archaea may be directly linked to eukaryotes. However, the genomes of Bacteria and non-Asgard Archaea generally organize ribosome-related genes into clusters that likely function as operons. In contrast, eukaryotes typically do not employ an operon strategy. To gain further insight into conservation of the r-protein genes, the genome order of conserved ribosomal protein (r-protein) coding genes was identified in 17 Asgard genomes (thirteen complete genomes and four genomes with less than 20 contigs) and compared with those found previously in non-Asgard archaeal and bacterial genomes. A universal core of two clusters of 14 and 4 cooccurring r-proteins, respectively, was identified in both the Asgard and non-Asgard Archaea. The equivalent genes in the E. coli version of the cluster are found in the S10 and spc operons. The large cluster of 14 r-protein genes (uS19-uL22-uS3-uL29-uS17 from the S10 operon and uL14-uL24-uL5-uS14-uS8-uL6-uL18-uS5-uL30-uL15 from the spc operon) occurs as a complete set in the genomes of thirteen Asgard genomes (five Lokiarchaeotes, three Heimdallarchaeotes, one Odinarchaeote, and four Thorarchaeotes). Four less conserved clusters with partial bacterial equivalents were found in the Asgard. These were the L30e (str operon in Bacteria) cluster, the L18e (alpha operon in Bacteria) cluster, the S24e-S27ae-rpoE1 cluster, and the L31e, L12..L1 cluster. Finally, a new cluster referred to as L7ae was identified. In many cases, r-protein gene clusters/operons are less conserved in their organization in the Asgard group than in other Archaea. If this is generally true for nonribosomal gene clusters, the results may have implications for the history of genome organization. In particular, there may have been an early transition to or from the operon approach to genome organization. Other nonribosomal cellular features may support different relationships. For this reason, it may be important to consider ribosome features separately.