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

Abstract

RNase P, an essential housekeeping endonuclease needed for 5'-processing of tRNAs, exists in two distinct forms: one with an RNA- and the other with a protein-based active site. The notion that the protein form of RNase P exists only in eukaryotes has been upended by the recent discovery of a protein-only variant in Bacteria and Archaea. The use of these two divergent scaffolds, shaped by convergent evolution, in all three domains of life inspires questions relating to the ancestral form of RNase P, as well as their origins and function(s) in vivo. Results from our analysis of publicly available bacterial and archaeal genomes suggest that the widespread RNA-based ribonucleoprotein variant is likely the ancient form. We also discuss the possible genetic origins and function of RNase P, including how the simultaneous presence of its variants may contribute to the fitness of their host organisms.

Keywords: RNase P; convergent evolution; tRNA processing.

FIGURE 1.

Occurrence of HARP in bacterial and archaeal genomes. HARP homologs were identified using BLASTP and domain searches at the National Center for Biotechnology Information (NCBI) and Integrated Microbial Genomes and Microbiomes (IMG/M). Established bacterial and archaeal HARP sequences (Rosenblad et al. 2006; Nickel et al. 2017) were used as queries in BLASTP searches. BLASTP matches (E ≤ 10⁻²⁰ and bit scores >100) and members of the PIN_5/pfam08745, TIGR03875, or COG1458 families were selected as potential HARP homologs. Candidates identified using domain matches were verified by an independent BLASTP search. Genomes found to encode HARP were also examined for the occurrence of the RNase P RNP variant using as queries the bacterial RNase P protein RnpA and four archaeal RNase P proteins (POP5, RPP21, RPP29, and RPP30). (A) Taxonomic overview of HARP in bacterial and archaeal genomes. Bacteria are presented at the phylum level and Archaea as superphylum groupings (as described in Spang et al. 2017). Groups highlighted in blue have genomes encoding HARP. The number of genomes examined in each group is indicated in parentheses. (B) Occurrence of HARP in bacterial genera. This panel is an expanded view at the genus level of the number of genomes encoding HARP alone or in co-occurrence with RnpA; RnpA was detected in nearly all bacterial genomes. An additional 2919 unclassified bacterial genomes were examined for HARP and RNase P RNP proteins. These genomes are not assigned to any specific bacterial phyla and thus are not included in our taxonomic overview in A; however, some members encode potential HARP homologs, and are therefore listed in this panel. The number of genera in each phylum is provided to illustrate the limited presence of HARP within that phylum. The four archaeal RNase P proteins are absent from all bacterial genomes examined (data not shown). A full list of the genomes examined in this analysis is available at https://figshare.com/s/8089e9b333da30b69368.

FIGURE 2.

Presence of HARP in archaeal genomes. Genomes were queried for HARP as described in Figure 1 using BLASTP searches with known HARP sequences (Nickel et al. 2017), which have been identified as members of the PIN_5/pfam08745, TIGR03875, or COG1458 families. (A) Summary of the number of genomes and the fraction of genera whose genomes encode HARP in each archaeal superphylum. Most genomes are classified to the genus level, but many of the DPANN and Asgard organisms are described as Candidatus and were conditionally counted as genera in our analysis. Genomes were also queried for the bacterial RnpA and archaeal RNase P RNP proteins. 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. Organisms are grouped taxonomically by their superphylum affiliation (indicated by the inner ring and mirroring the color scheme in A) and presented at the genus level. Genera encoding HARP are highlighted in blue with the fraction of HARP-containing genomes within each genus listed in the outer ring. The asterisk (*) denotes the class Halobacteria (see text for details).