The Diversity of Ribonuclease P: Protein and RNA Catalysts with Analogous Biological Functions

Klemm, Bradley P.; Wu, Nancy; Chen, Yu; Liu, Xin; Kaitany, Kipchumba; Howard, Michael J.; Fierke, Carol A.

doi:10.3390/biom6020027

Cited by 67 publications

(73 citation statements)

References 208 publications

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“…protein-only RNase P | Aquifex aeolicus | tRNA processing | HARP T he architectural diversity of RNase P enzymes is unique: In Bacteria, Archaea, and in the nuclei and organelles of many Eukarya, RNase P is a complex consisting of a catalytic RNA subunit and a varying number of proteins (one in Bacteria, at least four in Archaea, and up to 10 in Eukarya) (1,2). A different type of RNase P was discovered more recently in human mitochondria (3) and, subsequently, in land plants and some protists (4,5).…”

mentioning

confidence: 99%

Minimal and RNA-free RNase P in Aquifex aeolicus

Nickel

Wäber

Gößringer

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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RNase P is an essential tRNA-processing enzyme in all domains of life. We identified an unknown type of protein-only RNase P in the hyperthermophilic bacterium Aquifex aeolicus: Without an RNA subunit and the smallest of its kind, the 23-kDa polypeptide comprises a metallonuclease domain only. The protein has RNase P activity in vitro and rescued the growth of Escherichia coli and Saccharomyces cerevisiae strains with inactivations of their more complex and larger endogenous ribonucleoprotein RNase P. Homologs of Aquifex RNase P (HARP) were identified in many Archaea and some Bacteria, of which all Archaea and most Bacteria also encode an RNA-based RNase P; activity of both RNase P forms from the same bacterium or archaeon could be verified in two selected cases. Bioinformatic analyses suggest that A. aeolicus and related Aquificaceae likely acquired HARP by horizontal gene transfer from an archaeon.protein-only RNase P | Aquifex aeolicus | tRNA processing | HARP T he architectural diversity of RNase P enzymes is unique: In Bacteria, Archaea, and in the nuclei and organelles of many Eukarya, RNase P is a complex consisting of a catalytic RNA subunit and a varying number of proteins (one in Bacteria, at least four in Archaea, and up to 10 in Eukarya) (1, 2). A different type of RNase P was discovered more recently in human mitochondria (3) and, subsequently, in land plants and some protists (4, 5). This form, termed proteinaceous or protein-only RNase P (PRORP), lacks any RNA subunit and consists of one or three (animal mitochondria) protein subunit(s); it is found in most branches of the eukaryotic phylogenetic tree (6).Bacterial RNase P enzymes identified so far are composed of a ∼400-nt-long catalytic RNA subunit (encoded by rnpB) and a small protein subunit of ∼14 kDa (encoded by rnpA) (7). However, no rnpA and rnpB genes were identified in the genome of Aquifex aeolicus or other Aquificaceae (8-12). The genetic organization of A. aeolicus tRNAs in tandem clusters and as part of ribosomal operons and the detection of tRNAs with canonical mature 5′-ends in total RNA extracts from A. aeolicus implied the existence of a tRNA 5′-maturation activity (9) that was indeed subsequently detected in cell lysates of A. aeolicus (11, 13). However, to date, the identity and biochemical composition of RNase P in A. aeolicus has remained enigmatic. Results and DiscussionHere, we pursued a classical biochemical approach to identify the RNase P of A. aeolicus. The purification procedure consisted of three consecutive chromatographic steps: anion exchange, hydrophobic interaction, and size exclusion chromatography (AEC, HIC, and SEC, respectively; Fig. 1A and SI Appendix, Figs. S1-S8). RNase P activity was assayed at all purification steps. To identify putative protein components of the enzyme, fractions with low and high RNase P activity from different purification steps were comparatively analyzed by step-gradient SDS/PAGE, and protein bands correlating with activity (Fig. 1B) were subjected to mass spectrometry. An example i...

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confidence: 99%

Minimal and RNA-free RNase P in Aquifex aeolicus

Nickel

Wäber

Gößringer

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…All of the larger natural RNA enzymes, such as RNAseP and the various self‐splicing introns, depend on site‐specific metal ion cofactors for chemical reactivity. Likewise, the various artificial RNA ligase and polymerase ribozymes, which rely on nucleoside triphosphate activation chemistry, are strict metalloenzymes with only poor tolerance towards metal ions other than Mg 2+ .…”

Section: The Role Of Metal Ions In Nucleic Acid Folding and Catalysismentioning

confidence: 99%

“…[75] However, althought he Tetrahymena group Ir ibozyme folds into an ative-like state in the presence of various counterions, foldingo ft he catalytically active state requires site-specific binding of Mg 2 + or Mn 2 + . [75] All of the larger natural RNA enzymes,s uch as RNAseP [9,10] and the variouss elf-splicing introns, [15,16] depend on site-specific metal ion cofactors for chemical reactivity.L ikewise, the various artificial RNA ligase and polymerase ribozymes, which rely on nucleoside triphosphate activation chemistry,a re strict metalloenzymes with only poor tolerance towards metal ions other than Mg 2 + . [80] In view of this, it is quite surprising that moderni ntracellular conditions are somewhat challenging for nucleic acid folding and activity due to low free Mg 2 + concentrationso fa pproximately 1mm.…”

Section: Modes Of Metal Ion-nucleic Acid Interactionmentioning

confidence: 99%

“…For RNA (ribozymes), the most iconic example is the ribosome, whose central role in peptide bond formation and thus protein synthesis designates it the most important ribozyme in modern biochemistry, and the most obvious “smoking gun” of an early RNA world predating modern biochemistry. Another ubiquitous ribozyme that is essential in all free‐living organisms is RNAseP, which processes the 5′‐ends of precursor‐tRNAs . Other prominent examples for ribozymes are small RNA‐cleaving ribozymes such as the hammerhead (HH) ribozyme (Figure A) and the hairpin (HP) ribozyme (Figure B), which catalyze reversible self‐cleavage to process the concatemeric products of rolling circle RNA replication into linear and circular RNA molecules .…”

Section: Introductionmentioning

confidence: 99%

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Nucleic Acid Catalysis under Potential Prebiotic Conditions

Vay

Salibi

Song

et al. 2019

Chemistry An Asian Journal

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Catalysis by nucleic acids is indispensable for extant cellular life, and it is widely accepted that nucleic acid enzymes were crucial fort he emergence of primitive life 3.5-4b illion years ago. However,g eochemicalc onditions on early Earth must have differed greatlyf rom the constant internal milieus of today's cells. In order to explore plausible scenarios for early molecular evolution, it is therefore essential to understand how different physicochemical parame-ters, such as temperature,p H, and ionic composition, influence nucleic acidc atalysis and to explore to what extent nucleic acid enzymes can adapt to non-physiological conditions. In this article, we give an overview of the research on catalysis of nucleic acids, in particularc atalytic RNAs (ribozymes) and DNAs( deoxyribozymes), under extreme and/or unusualc onditions that may relate to prebiotic environments.[a] Dr.

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“…The 5 0 leader of tRNA precursors is universally removed by an endonuclease called RNase P. 8,[13][14][15][16] The enzyme is found in one of 2 fundamentally different forms: either as a ribonucleoprotein based on a catalytic RNA molecule, or as a pure protein enzyme; 8,[13][14][15][16] both nevertheless function in an essentially similar way and are experimentally exchangeable. 17 With the exception of some tRNAs His in Eukarya (see below), RNase P forms the final, mature 5 0 end of tRNAs by a precise endonucleolytic cut.…”

Section: Introductionmentioning

confidence: 99%