Comprehensive classification of the PIN domain-like superfamily

Matelska, Dorota; Steczkiewicz, Kamil; Ginalski, Krzysztof

doi:10.1093/nar/gkx494

Cited by 89 publications

(93 citation statements)

References 213 publications

(247 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…S22-S24 and Table S1), but none in Eukarya. We therefore propose to name this type of protein-only RNase P "HARP" for Homolog of Aquifex RNase P. The HARP proteins fall within the PIN_5 group of a recently published classification of the PIN domain-like superfamily (21). The relatively large group of archaeal organisms that encode HARP (SI Appendix, Table S1) have in common that they additionally encode an RNP RNase P. This suggests at least partially divergent functions of HARP and RNP enzymes in these Archaea, rather than reflecting evolutionary transition states where RNP RNase P is about to be replaced by HARP.…”

Section: Resultsmentioning

confidence: 99%

Minimal and RNA-free RNase P in Aquifex aeolicus

Nickel

Wäber

Gößringer

et al. 2017

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

View full text Add to dashboard Cite

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...

show abstract

Section: Resultsmentioning

confidence: 99%

Minimal and RNA-free RNase P in Aquifex aeolicus

Nickel

Wäber

Gößringer

et al. 2017

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

View full text Add to dashboard Cite

show abstract

“…Transcriptome and proteome data of M. mazei indicate co-expression of HARP (Mm_2077) and RNA-based RNase P subunits (Mm_1556 = Rpp21, Mm_2132 = Rpp29, Mm_2618 = Rpp30, Mm_2619 = Pop5, Mm_2467 = L7Ae) (unpublished data). The HARPs are evolutionarily linked to toxin-antitoxin systems in bacteria and archaea (20), where the toxin proteins are often sequence-specific endoribonucleases that degrade mRNA, rRNA, tmRNA or tRNA to inhibit protein biosynthesis in response to certain stresses (28). For example, proteins with a PIN domain-like fold of the VapC (virulence-associated protein C) type include VapC endonucleases from Shigella flexneri and Salmonella enterica Typhimurium LT2 that specifically cleave initiator-tRNA fMet (but not elongator tRNAs including tRNA Met ) in the anticodon loop at the junction to the 3 0 -strand of the anticodon stem (29).…”

Section: Discussionmentioning

confidence: 99%

Homologs of aquifex aeolicus protein‐only RNase P are not the major RNase P activities in the archaea haloferax volcanii and methanosarcina mazei

et al. 2019

View full text Add to dashboard Cite

The mature 5′‐ends of tRNAs are generated by RNase P in all domains of life. The ancient form of the enzyme is a ribonucleoprotein consisting of a catalytic RNA and one or more protein subunits. However, in the hyperthermophilic bacterium Aquifex aeolicus and close relatives, RNase P is a protein‐only enzyme consisting of a single type of polypeptide (Aq_880, ~23 kDa). In many archaea, homologs of Aq_880 were identified (termed HARPs for Homologs of Aquifex RNase P) in addition to the RNA‐based RNase P, raising the question about the functions of HARP and the classical RNase P in these archaea. Here we investigated HARPs from two euryarchaeotes, Haloferax volcanii and Methanosarcina mazei. Archaeal strains with HARP gene knockouts showed no growth phenotypes under standard conditions, temperature and salt stress (H. volcanii) or nitrogen deficiency (M. mazei). Recombinant H. volcanii and M. mazei HARPs were basically able to catalyse specific tRNA 5′‐end maturation in vitro. Furthermore, M. mazei HARP was able to rescue growth of an Escherichia coli RNase P depletion strain with comparable efficiency as Aq_880, while H. volcanii HARP was unable to do so. In conclusion, both archaeal HARPs showed the capacity (in at least one functional assay) to act as RNases P. However, the ease to obtain knockouts of the singular HARP genes and the lack of growth phenotypes upon HARP gene deletion contrasts with the findings that the canonical RNase P RNA gene cannot be deleted in H. volcanii, and a knockdown of RNase P RNA in H. volcanii results in severe tRNA processing defects. We conclude that archaeal HARPs do not make a major contribution to global tRNA 5′‐end maturation in archaea, but may well exert a specialised, yet unknown function in (t)RNA metabolism. © 2019 IUBMB Life, 2019 © 2019 IUBMB Life, 71(8):1109–1116, 2019

show abstract

“…The VapC toxins are characterized by the presence of a PIN domain that presents a structural similarity with the classical Rossmann-fold associated with the binding of nucleotides and nucleotide-based cofactors (Rao and Rossmann, 1973;Matelska et al, 2017;Senissar et al, 2017). The PIN domain, although originally owing its name to the type IV pili protein PilT (PilT N-terminal like nucleases), is generally found in proteins that present various endonuclease functions such as tRNA and rRNA maturation, nonsense mediated mRNA decay, and DNA replication and repair in all domains of life (Matelska et al, 2017;Senissar et al, 2017). In the PIN motif, alternating beta strands and alpha helices (α/β/α sandwich) fold into a central five stranded parallel beta-sheet decorated with alpha helices on both sides (Figure 3).…”

Section: Vapc Toxinsmentioning

confidence: 99%

The Variety in the Common Theme of Translation Inhibition by Type II Toxin–Antitoxin Systems

Jurėnas

Melderen

2020

Front. Genet.

View full text Add to dashboard Cite

Type II Toxin-antitoxin (TA) modules are bacterial operons that encode a toxic protein and its antidote, which form a self-regulating genetic system. Antitoxins put a halter on toxins in many ways that distinguish different types of TA modules. In type II TA modules, toxin and antitoxin are proteins that form a complex which physically sequesters the toxin, thereby preventing its toxic activity. Type II toxins inhibit various cellular processes, however, the translation process appears to be their favorite target and nearly every step of this complex process is inhibited by type II toxins. The structural features, enzymatic activities and target specificities of the different toxin families are discussed. Finally, this review emphasizes that the structural folds presented by these toxins are not restricted to type II TA toxins or to one particular cellular target, and discusses why so many of them evolved to target translation as well as the recent developments regarding the role(s) of these systems in bacterial physiology and evolution.

show abstract

Comprehensive classification of the PIN domain-like superfamily

Cited by 89 publications

References 213 publications

Minimal and RNA-free RNase P in Aquifex aeolicus

Minimal and RNA-free RNase P in Aquifex aeolicus

Homologs of aquifex aeolicus protein‐only RNase P are not the major RNase P activities in the archaea haloferax volcanii and methanosarcina mazei

The Variety in the Common Theme of Translation Inhibition by Type II Toxin–Antitoxin Systems

Contact Info

Product

Resources

About