Molecular Evolution of the Archaeal DNA-Dependent RNA Polymerase: Cooperative Changes in Subunit Composition and Specific Domains of Small Subunits

The subunit composition and tertiary structure of DNA-dependent RNA polymerases in archaea, bacteria, and eukaryotes are currently well understood. The single RNA polymerase of archaea resembles the nuclear RNA polymerase II of eukaryotes in its composition and consists of 10–12 subunits. Perhaps the only exception that seems to confirm this rule is the Rpo8 subunit (homologue of the eukaryotic Rpb8), which only some classes of archaea have. The development of metagenomic sequencing has led to a significant revision of the classification system of prokaryotes, in particular to the identification of a number of new Archaea evolutionary lineages. This makes it possible to analyze the subunit composition and structure of RNA polymerase of all currently isolated archaeal phyla. Our analysis shows that the Rpo8 subunit is present only in the RNA polymerase of Archaea species from the Thermoproteota of the Thermoproteati superphylum and from the whole superphylum Promethearchaeati, formerly known as the Asgard. After analyzing the changes in the small Rpo6 subunit (homologue of eukaryotic Rpb6), functionally interacting with Rpo8, we noticed that the largest number of changes in the primary and domain structures of this small subunit occurred in archaeal phyla that lack Rpo8. Shortened forms of Rpo6 without N- or C-terminal regions were observed only in representatives of archaea with an RNA polymerase that does not contain the Rpo8 subunit. Our analysis shows that the changes in Rpo6 are an adaptation of a multisubunit transcription complex to the disappearance of Rpo8. Most likely, the Rpo8 subunit was present in the RNA polymerase of the Last Common Ancestor of Archaea (LCAA) and, in the course of evolution, disappeared in the superphyla Euryarchaeota and Nanobdellati and two divisions of the Thermoproteati superphylum: Bathyarchaeota and Thaumarchaeota.