New developments in post-transcriptional regulation of operons by small RNAs

Balasubramanian, Divya; Vanderpool, Carin K.

doi:10.4161/rna.23696

Cited by 29 publications

(28 citation statements)

References 42 publications

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“…Regulation by sRNAs targeting the 5'UTR and masking the RBS leading to inhibition of translation initiation is well-known in bacteria (Desnoyers et al, 2013). Targeting one or selected internal RBS in a polycistronic mRNA can lead to discoordinated expression of the respective genes, as has been shown, e.g., for Spot42 from Escherichia coli, exclusively affecting GalK level in the galETKM operon by targeting the RBS of galK (Balasubramanian and Vanderpool, 2013). In Archaea, regulatory mechanisms have been identified only for a few sRNAs at the molecular level.…”

Section: Discussionmentioning

confidence: 99%

sRNA₄₁ affects ribosome binding sites within polycistronic mRNAs in Methanosarcina mazei Gö1

Buddeweg

Sharma

Urlaub

et al. 2018

Molecular Microbiology

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Several noncoding RNAs potentially involved in nitrogen (N)-regulation have been detected in Methanosarcina mazei, however, targets have been identified only for one of them. Here, we report on the function of sRNA , highly expressed under N-sufficiency. Comprising 120 nucleotides, sRNA shows high sequence and structural conservation within draft genomes of numerous Methanosarcina species. In silico target prediction revealed several potential targets, including genes of two homologous operons encoding for acetyl-CoA-decarbonylase/synthase complexes (ACDS) representing highly probable target candidates. A highly conserved single stranded region of sRNA was predicted to mask six independent ribosome binding sites of these two polycistronic mRNAs and was verified in vitro by microscale thermophoresis. Proteome analysis of the respective sRNA -deletion mutant showed increased protein expression of both ACDS complexes in the absence of sRNA , whereas no effect on transcript levels was detected, arguing for sRNA -mediated post-transcriptional fine-tuning of ACDS expression. We hypothesize that the physiological advantage of downregulating sRNA under N-limiting conditions is the resulting increase of ACDS protein levels. This provides sufficient amounts of amino acids for nitrogenase synthesis as well as reducing equivalents and energy for N -fixation, thus linking the carbon and N-metabolism.

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Section: Discussionmentioning

confidence: 99%

sRNA₄₁ affects ribosome binding sites within polycistronic mRNAs in Methanosarcina mazei Gö1

Buddeweg

Sharma

Urlaub

et al. 2018

Molecular Microbiology

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“…QfsR represses exo polycistronic mRNA and activates flg and traI-trb polycistronic mRNAs (Table 1, Figure 3). Whatever the targets, QfsR directly interacts within the polycistronic molecule and coordinates expression of its encoded genes (Table 1, Figure 2), highlighting the involvement of QfsR in the regulation of polycistronic mRNAs (49). Additional studies are necessary to decipher the mechanism involved.…”

Section: Discussionmentioning

confidence: 99%

A novel plasmid-transcribed regulatory sRNA, QfsR, controls chromosomal polycistronic mRNAs in Agrobacterium tumefaciens

Diel

Dequivre

Wisniewski‐Dyé

et al. 2019

Preprint

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21Plasmids are mobile DNAs that adjust host cell functions for their own amplification and dissemination. 22We identified QfsR, a small RNA, transcribed from the Ti plasmid in the phytopathogen Agrobacterium 23 fabrum. QfsR is widely conserved throughout RepABC plasmids carried by Rhizobiaceae. Target 24 prediction, expression analysis and site-direct mutagenesis experiments show that QfsR directly pairs 25 within polycistronic mRNAs transcribed from chromosomes (involved in flagella apparatus and 26 succinoglycan biosynthesis) and Ti plasmid (involved in conjugative transfer). QfsR leads to a 27 coordinated expression of whole polycistronic mRNA molecules. Whereas a lack of QfsR induces 28 motility and reduces succinoglycan production, its overproduction increases the quorum sensing signal 29 accumulation and the Ti plasmid conjugative transfer. Based on these observations, we propose QfsR 30 as a hub connecting regulatory networks of motility, succinoglycan biosynthesis and plasmid 31 conjugative transfer. To our knowledge, QfsR is the first example of a plasmid-encoded sRNA that 32 controls chromosomal polycistronic mRNAs. 33 Significance 34Plasmids represent an important cost for the hosting cell although some are beneficial under certain 35 circumstances. Agrobacterium tumefaciens harboring Tumor inducing plasmid (pTi) are able to infect 36 plants and to use specific resources produced by the infected cells. We characterized QfsR, a novel small 37 RNA (sRNA) from pTi, that directly regulates plasmid polycistronic mRNA but also chromosomal ones. 38QfsR contributes to a fine-tuned regulation of bacterial motility, exopolysaccharide biosynthesis and 39 conjugative dissemination of pTi. Our results report the first plasmid-encoded sRNA able to modify and 40 coordinate cellular behaviour probably for the benefit of the plasmid dissemination and tight crosstalk 41 between plasmid and chromosome. This could be widespread since QfsR homologs were predicted in 42 other plasmids of Rhizobiaceae symbionts and pathogens. 44 45Plasmids are foreign DNAs whose expression and replication can impose a significant cost on host cells. 46However, their acquisition might be beneficial under certain circumstances, conferring advantageous 47 traits, such as antibiotic resistance, ability to catabolize nutrients, and pathogenesis (1)(2)(3). To reduce 48 fitness cost, both plasmid and host cells have developed a tight regulatory network, which may involve 49 crosstalk between chromosome and plasmid. Indeed, several chromosomal regulators control the 50 expression of plasmid functions (4)(5) and more rarely plasmid regulators control chromosomal genes 51 (6)(7)(8). 52Agrobacterium with the Tumor inducing (Ti) plasmid is responsible for bacterial virulence on a variety 53 of dicotyledonous plants, as it induces the production of plant growth hormones that cause cell 54 proliferation (tumours) (9). The major virulence factors encoded by the Ti plasmid include a type IV 55 secretion system and accessory proteins (TSS4 and Vir) responsib...

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“…This seems contradictory to the operon-like genomic organization of the genes. However, it has been shown that the expression of genes in an operon can be discoordinately regulated by means of small noncoding RNAs (sRNAs) (Balasubramanian and Vanderpool 2013). In the case of pyocin S6, such a discoordinate regulatory mechanism might protect the bacterial cell from spending energy in the production of the pyocin molecule, while under ironlimiting conditions, when the target receptors are abundantly expressed, a different regulatory mechanism may stabilize the pyocin transcript.…”

Section: Discussionmentioning

confidence: 99%

Identification and functional analysis of a bacteriocin, pyocin S6, with ribonuclease activity from a Pseudomonas aeruginosa cystic fibrosis clinical isolate

et al. 2016

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S‐type pyocins are bacteriocins produced by Pseudomonas aeruginosa isolates to antagonize or kill other strains of the same species. They have a modular organization comprising a receptor‐binding domain recognizing a surface constituent of the target bacterium, a domain for translocation through the periplasm, and a killing or toxic domain with DNase, tRNase, or pore‐forming activity. Pyocins S2, S3, S4, and S5 recognize TonB‐dependent ferri‐siderophore receptors in the outer membrane. We here describe a new nuclease bacteriocin, pyocin S6, encoded in the genome of a P. aeruginosa cystic fibrosis (CF) clinical isolate, CF_PA39. Similarly to pyocins S1 and S2, the S6 toxin–immunity gene tandem was recruited to the genomic region encoding exotoxin A. The pyocin S6 receptor‐binding and translocation domains are identical to those of pyocin S1, whereas the killing domain is similar to the 16S ribonuclease domain of Escherichia coli colicin E3. The cytotoxic activity was abolished in pyocin S6 forms with a mutation in the colicin E3‐equivalent catalytic motif. The CF_PA39 S6 immunity gene displays a higher expression level than the gene encoding the killing protein, the latter being only detected when bacteria are grown under iron‐limiting conditions. In the S1‐pyocinogenic strain P. aeruginosa ATCC 25324 and pyocin S2 producer P. aeruginosa PAO1, a remnant of the pyocin S6 killing domain and an intact S6‐type immunity gene are located downstream of their respective pyocin operons. Strain PAO1 is insensitive for pyocin S6, and its S6‐type immunity gene provides protection against pyocin S6 activity. Purified pyocin S6 inhibits one‐fifth of 110 P. aeruginosa CF clinical isolates tested, showing clearer inhibition zones when the target cells are grown under iron limitation. In this panel, about half of the CF clinical isolates were found to host the S6 genes. The pyocin S6 locus is also present in the genome of some non‐CF clinical isolates.

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New developments in post-transcriptional regulation of operons by small RNAs

Cited by 29 publications

References 42 publications

sRNA₄₁ affects ribosome binding sites within polycistronic mRNAs in Methanosarcina mazei Gö1

sRNA₄₁ affects ribosome binding sites within polycistronic mRNAs in Methanosarcina mazei Gö1

A novel plasmid-transcribed regulatory sRNA, QfsR, controls chromosomal polycistronic mRNAs in Agrobacterium tumefaciens

Identification and functional analysis of a bacteriocin, pyocin S6, with ribonuclease activity from a Pseudomonas aeruginosa cystic fibrosis clinical isolate

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New developments in post-transcriptional regulation of operons by small RNAs

Cited by 29 publications

References 42 publications

sRNA41 affects ribosome binding sites within polycistronic mRNAs in Methanosarcina mazei Gö1

sRNA41 affects ribosome binding sites within polycistronic mRNAs in Methanosarcina mazei Gö1

A novel plasmid-transcribed regulatory sRNA, QfsR, controls chromosomal polycistronic mRNAs in Agrobacterium tumefaciens

Identification and functional analysis of a bacteriocin, pyocin S6, with ribonuclease activity from a Pseudomonas aeruginosa cystic fibrosis clinical isolate

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sRNA₄₁ affects ribosome binding sites within polycistronic mRNAs in Methanosarcina mazei Gö1

sRNA₄₁ affects ribosome binding sites within polycistronic mRNAs in Methanosarcina mazei Gö1