Novel One-step Mechanism for tRNA 3′-End Maturation by the Exoribonuclease RNase R of Mycoplasma genitalium

Alluri, Ravi Kumar; Li, Zhongwei

doi:10.1074/jbc.m111.324970

Cited by 12 publications

(11 citation statements)

References 23 publications

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“…Finally, because the terminal 3′-CCA sequence of mature tRNAs in all Mollicutes species are generally encoded in the genome [73] , the tRNA nucleotidyl transferase (CCAase) became obsolete and the pre-tRNA processing machinery exactly trims the tRNA at the CCA end with one RNase only [74] , while in other bacteria several accessory RNases are needed (see below). The loss of the encoded CCAase gene occurred very early in Mollicutes evolution (node 37, Figure 3 ).…”

Section: Resultsmentioning

confidence: 99%

“…RNase III, is the only enzyme involved in sizing RNA precursors within their double-stranded regions [115] , while RNase R and YbeY/YqfG remove the 3′-tails of tRNA and 16S-rRNA precursors, respectively. RNase R of M. genitalium removes the 3′-trailer in pre-tRNA in only one step [74] , a process requiring an interplay of multiple enzymes in other bacteria. Thus because RNase R has become more selective during Mollicutes genomic erosion, several other RNase encoding genes have become dispensable.…”

Section: Resultsmentioning

confidence: 99%

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Predicting the Minimal Translation Apparatus: Lessons from the Reductive Evolution of Mollicutes

et al. 2014

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Mollicutes is a class of parasitic bacteria that have evolved from a common Firmicutes ancestor mostly by massive genome reduction. With genomes under 1 Mbp in size, most Mollicutes species retain the capacity to replicate and grow autonomously. The major goal of this work was to identify the minimal set of proteins that can sustain ribosome biogenesis and translation of the genetic code in these bacteria. Using the experimentally validated genes from the model bacteria Escherichia coli and Bacillus subtilis as input, genes encoding proteins of the core translation machinery were predicted in 39 distinct Mollicutes species, 33 of which are culturable. The set of 260 input genes encodes proteins involved in ribosome biogenesis, tRNA maturation and aminoacylation, as well as proteins cofactors required for mRNA translation and RNA decay. A core set of 104 of these proteins is found in all species analyzed. Genes encoding proteins involved in post-translational modifications of ribosomal proteins and translation cofactors, post-transcriptional modifications of t+rRNA, in ribosome assembly and RNA degradation are the most frequently lost. As expected, genes coding for aminoacyl-tRNA synthetases, ribosomal proteins and initiation, elongation and termination factors are the most persistent (i.e. conserved in a majority of genomes). Enzymes introducing nucleotides modifications in the anticodon loop of tRNA, in helix 44 of 16S rRNA and in helices 69 and 80 of 23S rRNA, all essential for decoding and facilitating peptidyl transfer, are maintained in all species. Reconstruction of genome evolution in Mollicutes revealed that, beside many gene losses, occasional gains by horizontal gene transfer also occurred. This analysis not only showed that slightly different solutions for preserving a functional, albeit minimal, protein synthetizing machinery have emerged in these successive rounds of reductive evolution but also has broad implications in guiding the reconstruction of a minimal cell by synthetic biology approaches.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Predicting the Minimal Translation Apparatus: Lessons from the Reductive Evolution of Mollicutes

et al. 2014

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“…In addition to the six exoribonucleases tested above, E. coli contains a seventh 3′ → 5′ exonuclease called RNase R, which is not inhibited by RNA secondary structure ( 37 ), requires a 7 nt single-stranded region for substrate binding ( 38 ), but has not been implicated in E. coli tRNA maturation. Even so, we investigated its potential involvement in the 3′ end processing of proK, proL and proM tRNAs, since it has been shown to participate in tRNA 3′ end processing in Mycoplasma genitalium ( 39 ). However, no effect of RNase R was observed in an Δrnr Δrnt Δrnd rph-1 multiple mutant (Figures 1 and 2 , lanes 5 and 13; Figure 3 , lane 5).…”

Section: Resultsmentioning

confidence: 99%

Endonucleolytic cleavages by RNase E generate the mature 3′ termini of the three proline tRNAs inEscherichia coli

2016

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We demonstrate here for the first time that proline tRNA 3′ end maturation in Escherichia coli employs a one-step endonucleolytic pathway that does not involve any of the six 3′ → 5′ exonucleases (RNase T, RNase PH, RNase D, RNase BN, RNase II and polynucleotide phosphorylase [PNPase]) to generate the mature CCA terminus. Rather, RNase E is primarily responsible for the endonucleolytic removal of the entire Rho-independent transcription terminator associated with the proK, proL and proM primary transcripts by cleaving immediately downstream of the CCA determinant. In the absence of RNase E, RNase G and RNase Z are weakly able to process the proK and proM transcripts, while PNPase and RNase P are utilized in the processing of proL. The terminator fragment derived from the endonucleolytic cleavage of proL transcript is degraded through a PNPase-dependent pathway. It is not clear which enzymes degrade the proK and proM terminator fragments. Our data also suggest that the mature 5′ nucleotide of the proline tRNAs may be responsible for the cleavage specificity of RNase E at the 3′ terminus.

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“…M. genitalium RNase R was shown to maturate tRNAs (46). E. coli RNase R is able to efficiently cleave 23 S and 16 S rRNAs but acts poorly on 5 S rRNA and tRNA (34).…”

Section: ϩmentioning

confidence: 99%

The RNase R from Campylobacter jejuni Has Unique Features and Is Involved in the First Steps of Infection

Haddad

Matos

Pinto

et al. 2014

Journal of Biological Chemistry

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Novel One-step Mechanism for tRNA 3′-End Maturation by the Exoribonuclease RNase R of Mycoplasma genitalium

Cited by 12 publications

References 23 publications

Predicting the Minimal Translation Apparatus: Lessons from the Reductive Evolution of Mollicutes

Predicting the Minimal Translation Apparatus: Lessons from the Reductive Evolution of Mollicutes

Endonucleolytic cleavages by RNase E generate the mature 3′ termini of the three proline tRNAs inEscherichia coli

The RNase R from Campylobacter jejuni Has Unique Features and Is Involved in the First Steps of Infection

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