Identification of a novel nanoRNase in Bartonella

Liu, Ma Feng; Cescau, Sandra; Mechold, Undine; Wang, Jing; Cohen, David; Danchin, Antoine; Boulouis, Henri-Jean; Biville, Francis

doi:10.1099/mic.0.054619-0

Cited by 34 publications

(40 citation statements)

References 33 publications

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“…This type of coupling between small molecules and macromolecule degradation will have to be taken into account in further developments of metabolic pathway tools and repositories. A further substantiation of this widespread category of pathways is seen with a similar double function, found for NrnC in alpha-proteobacteria (Liu et al, 2012), suggesting that this is an important metabolic feature of RNA catabolism. Another exonuclease of unknown specificity, YhaM, may also participate in the activity of the degradosome.…”

Section: Specific Genomic Objectssupporting

confidence: 61%

An updated metabolic view of the Bacillus subtilis 168 genome

Belda

Sekowska²,

Fèvre

et al. 2013

Microbiology

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Section: Specific Genomic Objectssupporting

confidence: 61%

An updated metabolic view of the Bacillus subtilis 168 genome

Belda

Sekowska²,

Fèvre

et al. 2013

Microbiology

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“…NrnA homologs are found in many bacteria that lack Orn (58). Additionally, another RNase with oligoribonuclease activity, NrnC, was recently identified in Bartonella birtlesii and is widely found in Alphaproteobacteria (59). Nearly all bacteria that encode diguanylate and diadenylate cyclases encode at least one RNase capable of degrading short oligoRNAs.…”

Section: Discussionmentioning

confidence: 99%

“…However, P. aeruginosa PA14 has no homologs of NrnA (56), NrnB (57), yhaM (expected value >1 in a protein BLAST search), RNase J1 (62), or NrnC (59). Other RNases may possess oligoribonuclease activity that partially compensates for the loss of orn.…”

Section: 6mentioning

confidence: 99%

Oligoribonuclease is the primary degradative enzyme for pGpG in Pseudomonas aeruginosa that is required for cyclic-di-GMP turnover

Orr

Donaldson

Severin

et al. 2015

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

121

142

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The bacterial second messenger cyclic di-GMP (c-di-GMP) controls biofilm formation and other phenotypes relevant to pathogenesis. Cyclic-di-GMP is synthesized by diguanylate cyclases (DGCs). Phosphodiesterases (PDE-As) end signaling by linearizing c-di-GMP to 5ʹ-phosphoguanylyl-(3ʹ,5ʹ)-guanosine (pGpG), which is then hydrolyzed to two GMP molecules by yet unidentified enzymes termed PDE-Bs. We show that pGpG inhibits a PDE-A from Pseudomonas aeruginosa. In a dual DGC and PDE-A reaction, excess pGpG extends the half-life of c-di-GMP, indicating that removal of pGpG is critical for c-di-GMP homeostasis. Thus, we sought to identify the PDE-B enzyme(s) responsible for pGpG degradation. A differential radial capillary action of ligand assay-based screen for pGpG binding proteins identified oligoribonuclease (Orn), an exoribonuclease that hydrolyzes two-to five-nucleotide-long RNAs. Purified Orn rapidly converts pGpG into GMP. To determine whether Orn is the primary enzyme responsible for degrading pGpG, we assayed cell lysates of WT and Δorn strains of P. aeruginosa PA14 for pGpG stability. The lysates from Δorn showed 25-fold decrease in pGpG hydrolysis. Complementation with WT, but not active site mutants, restored hydrolysis. Accumulation of pGpG in the Δorn strain could inhibit PDE-As, increasing c-di-GMP concentration. In support, we observed increased transcription from the c-di-GMP-regulated pel promoter. Additionally, the c-di-GMP-governed auto-aggregation and biofilm phenotypes were elevated in the Δorn strain in a pel-dependent manner. Finally, we directly detect elevated pGpG and c-di-GMP in the Δorn strain. Thus, we identified that Orn serves as the primary PDE-B enzyme that removes pGpG, which is necessary to complete the final step in the c-di-GMP degradation pathway.cyclic di-GMP | oligoribonuclease | pGpG | PDE-B | nanoRNase

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“…Apart from conserved sequence motifs necessary for activity, the sequences of nanoRNase families vary significantly. Consequently, sequence similarity of NrnC with NrnB and NrnA is only 16% and 11%, respectively (7). While NrnAs are bifunctional enzymes with nanoRNase and CysQ activity (313 residues in B. subtilis NrnA), only a nanoRNase activity has been identified in NrnB (399 residues in B. subtilis ) and NrnC (181 residues in B. birtlesii ).…”

Section: Introductionmentioning

confidence: 99%

Unique subunit packing in mycobacterial nanoRNase leads to alternate substrate recognitions in DHH phosphodiesterases

et al. 2014

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DHH superfamily includes RecJ, nanoRNases (NrnA), cyclic nucleotide phosphodiesterases and pyrophosphatases. In this study, we have carried out in vitro and in vivo investigations on the bifunctional NrnA-homolog from Mycobacterium smegmatis, MSMEG_2630. The crystal structure of MSMEG_2630 was determined to 2.2-Å resolution and reveals a dimer consisting of two identical subunits with each subunit folding into an N-terminal DHH domain and a C-terminal DHHA1 domain. The overall structure and fold of the individual domains is similar to other members of DHH superfamily. However, MSMEG_2630 exhibits a distinct quaternary structure in contrast to other DHH phosphodiesterases. This novel mode of subunit packing and variations in the linker region that enlarge the domain interface are responsible for alternate recognitions of substrates in the bifunctional nanoRNases. MSMEG_2630 exhibits bifunctional 3′-5′ exonuclease [on both deoxyribonucleic acid (DNA) and ribonucleic acid (RNA) substrates] as well as CysQ-like phosphatase activity (on pAp) in vitro with a preference for nanoRNA substrates over single-stranded DNA of equivalent lengths. A transposon disruption of MSMEG_2630 in M. smegmatis causes growth impairment in the presence of various DNA-damaging agents. Further phylogenetic analysis and genome organization reveals clustering of bacterial nanoRNases into two distinct subfamilies with possible role in transcriptional and translational events during stress.

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Identification of a novel nanoRNase in Bartonella

Cited by 34 publications

References 33 publications

An updated metabolic view of the Bacillus subtilis 168 genome

An updated metabolic view of the Bacillus subtilis 168 genome

Oligoribonuclease is the primary degradative enzyme for pGpG in Pseudomonas aeruginosa that is required for cyclic-di-GMP turnover

Unique subunit packing in mycobacterial nanoRNase leads to alternate substrate recognitions in DHH phosphodiesterases

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