Sequence Analysis and Comparative Study of the Protein Subunits of Archaeal RNase P

Abstract

RNase P, a ribozyme-based ribonucleoprotein (RNP) complex that catalyzes tRNA 5′-maturation, is ubiquitous in all domains of life, but the evolution of its protein components (RNase P proteins, RPPs) is not well understood. Archaeal RPPs may provide clues on how the complex evolved from an ancient ribozyme to an RNP with multiple archaeal and eukaryotic (homologous) RPPs, which are unrelated to the single bacterial RPP. Here, we analyzed the sequence and structure of archaeal RPPs from over 600 available genomes. All five RPPs are found in eight archaeal phyla, suggesting that these RPPs arose early in archaeal evolutionary history. The putative ancestral genomic loci of archaeal RPPs include genes encoding several members of ribosome, exosome, and proteasome complexes, which may indicate coevolution/coordinate regulation of RNase P with other core cellular machineries. Despite being ancient, RPPs generally lack sequence conservation compared to other universal proteins. By analyzing the relative frequency of residues at every position in the context of the high-resolution structures of each of the RPPs (either alone or as functional binary complexes), we suggest residues for mutational analysis that may help uncover structure-function relationships in RPPs.

Both kinds of RNase P in all domains of life: surprises galore

“…1 and 2). Indeed, a previous analysis of archaeal genomes indicated that all archaeal RNase P proteins are present in the majority of phyla, and support the hypothesis that the RNP form arose early in archaeal evolutionary history (Samanta et al 2016). In contrast, among the archaeal genomes examined, we observed that HARP is present in a wide range of Euryarchaeota genera, but absent in many of the TACK and all of the DPANN and Asgard groups ( Fig.…”

“…The bacterial RnpA was not found in any archaeal genome examined (data not shown). All archaeal genomes encode one or more of the RNP proteins, indicating evidence for the RNP form (Samanta et al 2016). (B) Analysis of archaeal genomes encoding HARP protein.…”

In vitro reconstitution and analysis of eukaryotic RNase P RNPs

“…Catalytically active archaeal RNase P can be reconstituted in vitro from proteins and RNA, which has enabled detailed studies of the interplay of its components ( 3 , 11 ). In archaeal RNase P, four of the proteins were shown to function as interacting pairs: Rpp30/aPop5 (yeast homologues are Rpp1/Pop5, Figure 1B ) and Rpp21/Rpp29 (yeast homologues are Rpr2/Pop4, Figure 1B ) ( 11 , 12 ). The Rpp30/aPop5 pair was shown to promote substrate cleavage and was suggested to have a functional overlap with the bacterial RNase P protein ( 15 , 16 ).…”

“…The nomenclature of structural elements is based on ( 13 ). (B) Protein components of archaeal RNase P from P. furiosus ( Pfu ) ( 12 ) and eukaryotic RNase P from S. cerevisiae ( 14 ). Arrows indicate homology between archaeal and yeast proteins.…”

Chance and necessity in the evolution of RNase P

“…The molecular masses of purified nuclear forms are ∼450 kDa. Intermediate in complexity is archaeal RNase P (∼200 kDa) composed of one RNA and up to five different protein subunits, whose presence in the genomes of at least eight of 11 archaeal phyla (Samanta et al 2016) reflects their origins early in archaeal evolutionary history. All archaeal RNase P proteins have homologs in eukaryotic RNase P (Fig.…”