Transcript decay mediated by RNase III in Borrelia burgdorferi

Snow, Santina; Bacon, Emily E.; Bergeron, Jennifer; Katzman, David; Wilhelm, Amelia R.; Lewis, Owen T.; Syangtan, Deepsing; Calkins, Andrew; Archambault, Linda; Anacker, Melissa; Schlax, Paula J.

doi:10.1016/j.bbrc.2020.05.201

Cited by 7 publications

(8 citation statements)

References 37 publications

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“…Two ribonucleases have been genetically characterized in B. burgdorferi: RNase III, encoded by the rnc gene (Anacker et al, 2018) and RNase Y, encoded by the essential rny gene (Drecktrah et al, 2020). RNase III, which recognizes and cleaves double-stranded RNA, is required for proper rRNA processing (Anacker et al, 2018) and for mRNA decay, at least for several transcripts (Snow et al, 2020), in the spirochete. RNase Y is involved in the biogenesis of 6S RNA in B. burgdorferi (Drecktrah et al, 2020), which has not been shown in any other bacterium, but the ribonuclease surely has additional roles in the cell, likely in the turnover of mRNA based on precedence in other bacteria (Lehnik-Habrink et al, 2011;Durand et al, 2012;Chen et al, 2013), as Bb6S RNA null mutants are viable but rny is essential for growth of the spirochete (Drecktrah et al, 2020).…”

Section: Rna Turnover and Ribonucleasesmentioning

confidence: 99%

“…Note that these studies are more complicated in B. burgdorferi because mRNA turnover in bacteria is generally quantified following inhibition of transcription with rifampicin, but the unusual RNA polymerase of B. burgdorferi is resistant to this antibiotic, so, instead, actinomycin D is used to arrest transcription (Archambault et al, 2013). The half-lives and steady-state levels of several mRNAs, as well as the steady-state levels of the stable rRNAs, were significantly increased in an rnc mutant, indicating a role for RNase III in RNA degradation (Snow et al, 2020). However, the steady-state levels of a couple mRNAs decreased in the rnc mutant, suggesting a more nuanced regulatory scheme involving RNase III.…”

Section: Rna Turnover and Ribonucleasesmentioning

confidence: 99%

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Gene Regulation and Transcriptomics

Samuels¹,

Lybecker²,

Yang³

et al. 2022

Current Issues in Molecular Biology

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Borrelia (Borreliella) burgdorferi, along with closely related species, is the etiologic agent of Lyme disease. The spirochete subsists in an enzootic cycle that encompasses acquisition from a vertebrate host to a tick vector and transmission from a tick vector to a vertebrate host. To adapt to its environment and persist in each phase of its enzootic cycle, B. burgdorferi wields three systems to regulate the expression of genes: the RpoN-RpoS alternative sigma (σ) factor cascade, the Hk1/Rrp1 twocomponent system and its product c-di-GMP, and the stringent response mediated by RelBbu and DksA. These regulatory systems respond to enzootic phase-specific signals and are controlled or finetuned by transcription factors, including BosR and BadR, as well as small RNAs, including DsrABb and Bb6S RNA. In addition, several other DNA-binding and RNA-binding proteins have been identified, although their functions have not all been defined. Global changes in gene expression revealed by highthroughput transcriptomic studies have elucidated various regulons, albeit technical obstacles have mostly limited this experimental approach to cultivated spirochetes. Regardless, we know that the spirochete, which carries a relatively small genome, regulates the expression of a considerable number of genes required for the transitions between the tick vector and the vertebrate host as well as the adaptation to each. caister.com/cimb 223 Curr. Issues Mol. Biol. Vol. 42 Curr. Issues Mol. Biol. 42: 223-266. caister.com/cimb Gene Regulation and Transcriptomics Samuels et al.Figure 2. A model of the RpoN-RpoS σ factor cascade. During tick feeding and mammalian infection, environmental and host signals activate the RpoN-RpoS σ factor cascade. Activation of RpoN requires phosphorylation of Rrp2 and accumulation of BosR. Rrp2 is the sole prokaryotic enhancer-binding protein present in B. burgdorferi that is required for RpoN (σ 54 ) activation. Phosphorylation of Rrp2 not only is required for RpoN-RpoS activation, but also is indispensable for cell survival, presumably replication. Levels of BosR respond to environmental signals and accumulation of BosR activates rpoS at its RpoN-dependent promoter via an unknown mechanism. BadR represses rpoS transcription by directly binding near the RpoN-dependent promoter region. In addition to the major rpoS mRNA species transcribed from the RpoN-dependent promoter, a longer rpoS transcript is produced at low cell density from an RpoN-independent promoter located within the upstream flgJ gene. The sRNA DsrABb regulates the efficiency of long rpoS mRNA species translation in response to temperature. DDB18 can regulate RpoS (σ S ) levels at the post-transcriptional level. Accumulation of rpoS transcript leads to the production of OspC, DbpA, DbpB, BBK32, and other mammalian infection-associated proteins.

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Section: Rna Turnover and Ribonucleasesmentioning

confidence: 99%

Section: Rna Turnover and Ribonucleasesmentioning

confidence: 99%

Gene Regulation and Transcriptomics

Samuels¹,

Lybecker²,

Yang³

et al. 2022

Current Issues in Molecular Biology

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“…The conservation of the RIIID within bacterial genomes allowed the identification of RNase III enzymes in the majority of bacterial species with, so far, the exception of Deinococcus radiodurans [6]. Similar to Ec-RNase III [18], RNase III is not essential in most bacteria (e.g., S. aureus [73], C. jejuni [69], Borrelia burgdorferi [74] or Synechococcus sp. strain PCC 7002 [55]).…”

Section: Bacterial Rnase IIImentioning

confidence: 99%

“…Hence in the absence of RNase III, the increased abundance of PNPase could compensate for the slower 16S rRNA maturation. It is worth noting that RNase III repression of PNPase expression is conserved in B. burgdorferi [74], S. coelicolor [156], S. pyogenes [157] and C. jejuni [158]. RNase III is also involved in the repression of the expression of the transcription factor NusA and the essential translation initiation factor IF2, which is also induced during a cold shock [159].…”

Section: Indirect Regulation Of Ribosome Biogenesismentioning

confidence: 99%

RNase III, Ribosome Biogenesis and Beyond

2021

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The ribosome is the universal catalyst for protein synthesis. Despite extensive studies, the diversity of structures and functions of this ribonucleoprotein is yet to be fully understood. Deciphering the biogenesis of the ribosome in a step-by-step manner revealed that this complexity is achieved through a plethora of effectors involved in the maturation and assembly of ribosomal RNAs and proteins. Conserved from bacteria to eukaryotes, double-stranded specific RNase III enzymes play a large role in the regulation of gene expression and the processing of ribosomal RNAs. In this review, we describe the canonical role of RNase III in the biogenesis of the ribosome comparing conserved and unique features from bacteria to eukaryotes. Furthermore, we report additional roles in ribosome biogenesis re-enforcing the importance of RNase III.

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“…A well‐studied example of the direct action of RNase III on mRNAs is the processing of the pnp transcript in many bacteria (Carzaniga et al, 2009; Gatewood et al, 2011; Portier et al, 1987; Régnier & Grunberg‐Manago, 1990; Snow et al, 2020). The pnp mRNA encodes the polynucleotide phosphorylase (PNPase), an important exoribonuclease with 3′ to 5′ phosphorolytic activity.…”

Section: Introductionmentioning

confidence: 99%

RNase III participates in control of quorum sensing, pigmentation and oxidative stress resistance in Rhodobacter sphaeroides

Börner,

Friedrich,

Klug

2023

Molecular Microbiology

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RNase III is a dsRNA‐specific endoribonuclease, highly conserved in bacteria and eukarya. In this study, we analysed the effects of inactivation of RNase III on the transcriptome and the phenotype of the facultative phototrophic α‐proteobacterium Rhodobacter sphaeroides. RNA‐seq revealed an unexpectedly high amount of genes with increased expression located directly downstream to the rRNA operons. Chromosomal insertion of additional transcription terminators restored wild type‐like expression of the downstream genes, indicating that RNase III may modulate the rRNA transcription termination in R. sphaeroides. Furthermore, we identified RNase III as a major regulator of quorum‐sensing autoinducer synthesis in R. sphaeroides. It negatively controls the expression of the autoinducer synthase CerI by reducing cerI mRNA stability. In addition, RNase III inactivation caused altered resistance against oxidative stress and impaired formation of photosynthetically active pigment‐protein complexes. We also observed an increase in the CcsR small RNAs that were previously shown to promote resistance to oxidative stress. Taken together, our data present interesting insights into RNase III‐mediated regulation and expand the knowledge on the function of this important enzyme in bacteria.

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Transcript decay mediated by RNase III in Borrelia burgdorferi

Cited by 7 publications

References 37 publications

Gene Regulation and Transcriptomics

Gene Regulation and Transcriptomics

RNase III, Ribosome Biogenesis and Beyond

RNase III participates in control of quorum sensing, pigmentation and oxidative stress resistance in Rhodobacter sphaeroides

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