- Research article
- Open Access
Escherichia coliYmdB regulates biofilm formation independently of its role as an RNase III modulator
© Kim et al.; licensee BioMed Central Ltd. 2013
- Received: 1 June 2013
- Accepted: 21 November 2013
- Published: 24 November 2013
Ribonuclease III (RNase III) activity modulates hundreds of genes in Escherichia coli (E. coli). YmdB, a member of the macrodomain protein family, is one of known trans-acting regulators of RNase III activity; however, the significance of its regulatory role in specific bacterial cellular processes and related genes has not been determined. YmdB overexpression was used to model YmdB-induced RNase III inhibition in vivo, and microarray analysis identified gene targets and cellular processes related to RNase III inhibition.
The expression of >2,000 E. coli genes was modulated by YmdB induction; 129 genes were strongly regulated, of which 80 have not been reported as RNase III targets. Of these, ten are involved in biofilm formation. Significantly, YmdB overexpression also inhibited biofilm formation via a process that is not uniquely dependent upon RNase III inhibition. Moreover, biofilm formation is interdependently regulated by RpoS, a known stress response regulator and biofilm inhibitor, and by YmdB.
This is the first global profile of target genes modulated by YmdB-induced RNase III inhibition in E. coli, and the data reveal a novel, hitherto unrecognized regulatory role for YmdB in biofilm modulation.
- Ribonuclease III (RNase III)
- Trans-acting regulator
- Escherichia coli
RNase III family members cleave double-stranded RNAs to yield 5′ phosphate and 3′ hydroxyl termini, and are extensively conserved in prokaryotes and eukaryotes [1–7]. During bacterial ribosome biogenesis, RNase III processes the ribosomal RNA (rRNA) precursors , and also mediates the maturation and/or degradation of different types of transcripts , small RNAs [10, 11], and mRNAs containing rnc[12, 13] or pnp genes . The structural and mechanistic features of RNase III have been extensively studied [1–14]; however, questions remain concerning the cellular control of RNase III activity under different physiological conditions.
In E. coli, some proteins are known as regulators for endo-RNase activity [15–18]. For example, RraA and RraB negatively regulate RNase E activity [15, 16]. In case of RNase III, bacteriophage T7 protein kinase  and YmdB  identified as an either activator or inhibitor of RNase III function. The activation process by bacteriophage T7 protein kinase is through binding to RNase III and phosphorylates the enzyme on serine . YmdB was the first RNase III-binding inhibitor to be identified in vivo using a novel genetic screening approach and, in common with other RNase regulators, YmdB expression is modulated by cold- or growth-stress . YmdB, acting in concert with other uncharacterized stress-mediated trans-acting factors, facilitates the regulation of RNase III activity under growth-  or osmotic stress conditions . Several protein identities are proposed for the trans-acting inhibitor(s) and potential targets of their inhibition has been suggested; for example, cellular targets of RNase III activity, such as the RNase III gene itself, rnc[12, 13], pnp, and rRNA processing by YmdB  and the level of bdm mRNA encoding a protein that promotes biofilm formation by unknown trans-acting factor(s) . The cellular processes required for RNase III inhibition by trans-acting factor(s) during stress responses are unclear; however, one post-transcriptional pathway has been proposed , which involves the general stress-responsive regulator, RpoS . By cleaving the rpoS mRNA 5′-leader , RNase III reduces RpoS production; the presence of YmdB limits this reaction and as a consequence, increases RpoS levels, which supports entry into the stationary phase . This hypothesis behind this process came from a study that used an RNase III mutant ; however, to clarify and identify new targets of RNase III inhibition, it is essential to adopt a model that mimics physiological RNase III inhibition via the induction of trans-acting factor(s).
The present study investigated RNase III inhibition via the ectopic expression of the regulatory protein, YmdB, and identified novel targets of inhibition. We also explored the mechanism(s) by which biofilm formation is regulated. Gene expression profiling of the entire E. coli open reading frame (ORF) following YmdB overexpression was performed using DNA microarray analysis, and revealed that ~2,000 transcripts were modulated. Of these, 129 genes spanning ten cellular processes were strongly modulated by YmdB expression. About 40 of these were similarly controlled by RNase III, including five novel targets. Moreover, among the YmdB-modulated genes, ten are reported to be related to biofilm formation, the presence of which is a universal feature of bacteria and a component of multicellular communities . Biochemical analyses indicate that induction of YmdB strongly inhibits biofilm formation in a manner similar to that of RpoS, which is a regulator of general stress responses  and a biofilm inhibitor [23–25]. Inhibition occurred via two mechanisms that were either dependent or independent of RNase III activity. Genetic studies revealed that the YmdB- and RpoS-induced decrease in biofilm formation required RpoS and YmdB, respectively. In conclusion, we have identified a novel role for YmdB as a modulator of biofilm formation, and revealed how a trans-acting factor can regulate RNase III activity, as well as function independently to enable a rapid response to changing cellular needs.
Bacterial strains, plasmids, primers, and growth conditions
Details of the bacterial strains and plasmids used are given in Additional file 1: Table S1. Primers used for qPCR analysis and DNA sequencing were synthesized by Bioneer (Korea) (Additional file 1: Table S2). All established mutant strains or chromosomal lacZ fusions were derived from E. coli BW25113. Analysis of rpoS promoter activity was based on a plasmid, pKSK001, containing promoter region −92 to +10 of the rpoS gene from the E. coli K12 genome (GenBank U00096.2) sub-cloned into the lacZ transcriptional fusion vector, pSP417 , after linearization by EcoRI/BamHI. The lacZ fusion in pKSK001 was recombined onto the chromosome (KSK003) using the transducing λ phage system, λRS45 , via a double recombination event and was verified as previously described . Strain ΔymdB was constructed by eliminating the kanamycin cassette (ymdB::km R ) from Keio-ΔymdB as described previously . Verification of Keio-ΔymdB, ΔymdB (KSK002), Keio-ΔrpoS, or rnc14∙Keio-ΔrpoS (KSK005) was carried out by colony PCR using primer pairs ymdB-F/-R or rpoS-F/-R and Emerald PCR premix (Takara) (Additional file 1: Figure S1), and the PCR products were read by DNA sequencing analysis using the same primers (data not shown). Verification of RNase III mutation was confirmed by Western blot analysis using antibodies against RNase III (Additional file 1: Figure S1). Bacteria were grown in Luria-Bertani (LB) broth or on LB plates at 37°C throughout this study. Antibiotics were used at the following concentrations: kanamycin, 50 μg/mL; tetracycline, 10 μg/mL; and chloramphenicol, 30 μg/mL.
Total RNA was extracted from IPTG (0.1 mM final concentration)-induced E. coli BW25113 cells (at an OD600 of 1.0) containing either pCA24N (−gfp) or ASKA-ymdB (−) using an RNeasy® Kit (Qiagen) with two additional DNase treatments. The integrity of the bacterial total RNA was checked by an Agilent 2100 Bioanalyzer. The cDNA probes were prepared by reverse transcription with random priming of total RNA (25 μg) in the presence of aminoallyl-dUTP for 3 h, followed by coupling of probes with Cy3 dye (for the reference) or Cy5 dye (for the test sample) (AP Biotech). The Cy3- or Cy5-labeled cDNA probes were purified, dried, and resuspended in hybridization buffer containing 30% formamide, 5× SSC, 0.1% SDS, and 0.1 mg/mL salmon sperm DNA. The cDNA probes were mixed together and hybridized to customized microarray slides (E. coli K12 3 × 15 K microarray; http://www.mycroarray.com). The image of the slide was scanned with a GenePix 4000B (Axon Instruments, USA) and analyzed by GenePix Pro 3.0 software (Axon Instruments) to obtain the gene expression ratios (reference vs. test sample). Microarray data analysis was performed using Genowiz 4.0™ (Ocimum Biosolutions). Global lowess (Locally weighted scatter plot smoothing) method was used for data normalization. The cut-off values for up- or down-regulated genes in duplicate hybridizations were 1.5- or 0.6-fold, respectively.
The E. coli strains listed in Additional file 1: Table S1 were grown in LB medium to an OD600 of 1.0, and the total RNA was extracted using an RNeasy Mini Kit (Qiagen). Reverse transcription and qPCR (RT-qPCR) analyses were performed using CFX96 (Bio-Rad) with IQ™ SYBR® Green Supermix (Bio-Rad), as described previously  and gene specific primers designed by PrimerQuest (http://www.idtdna.com; Additional file 1: Table S2). Primer-dimer and self-complementary formations were checked by melting curve analysis (CFX manager v3.0; Bio-Rad). The 16S rRNA primers were used for normalization .
Crystal violet biofilm assay
The assay was adapted from Nakao et al. with the following modifications: E. coli were grown in LB broth for 16 h at 37°C and diluted to 5 × 106 CFU/mL in fresh LB broth with or without IPTG. Aliquots (800 μL) dispensed into polystyrene tubes (Falcon 352058, BD Biosciences) and incubated for 24 h at 37°C without shaking. Each data point represents the mean ± standard deviation of ten independent cultures.
β-galactosidase activity assays
The β-galactosidase activity from whole cells of KSK003 (λrpoS’-‘lacZ), KSK004 [SG30013 (λRpoS750::LacZ)] , RS8872 (λpnp’-‘lacZ in rnc+) , or RS8942 (λpnp’-‘lacZ in rnc14)  overexpressing YmdB from ASKA-ymdB (−) was determined as described by Miller . The results are expressed as the means of three independent experiments.
Protein gel electrophoresis and Western blot analysis
Overexpression of the YmdB and RpoS proteins was detected on Coomassie blue-stained 12% Mini-PROTEAN TGX Precast gels (Bio-Rad). Western blots for RNase III, YmdB, RpoS, or 6x Histidine-tagged YmdB were prepared as described , probed with antibodies (1:2,500 dilution) against YmdB, RNase III , RpoS (1RS1: Santa Cruz Biotechnology), or 6x Histidine-tagged YmdB (6xHis Epitope Tag Antibody: Thermo Scientific) and developed with Clarity™ western ECL substrate (Bio-Rad). To normalize the signals, antibodies against S1 protein  was used as a reference probe (1:100,000 dilution). Anti-rabbit IgG:HRP or anti-mouse IgG:HRP conjugates (Promega; 1:5000 dilution) were used for YmdB/RNase III/S1 proteins or RpoS/6xHistidine tagged YmdB, respectively. Specific proteins were imaged using MyECL and quantified with myImage Analysis software (Thermo Scientific).
Analysis of the E. coli transcriptome under conditions mimicking those of an RNase III mutant
Classification of up- or down-regulated 80 genes when YmdB was overexpressed
No. of gene
Go term ID
dppA, emrA, exbB, exuT, fdx, fecI, gutM, icd, mntH, nrfA 2 , proP, srlA 2 , srlB 2 , srlE 2 , srlR, sucA 2 , sucC 2 , sucD 2 , tdcC, tolB, tolR, yhbE, ynfM
cspB, cspG, fecI, gutM, lacI, mprA, mukF, mqsR 3 , pspB 1,2 , pspC 1,3 , relE 3 , rpoA, rpoB, rpoC, rplD, rpoE 3 , rseB, srlR, yoeB, ygiT 3
cspB, cspG, emrA, mprA, nusA, pspB 1,3 , pspC 1,3 , pspD 1,3 ,
relE 3 , rplD, rpoE 3 , rseA 3 , sseA
csdA, iscA, iscU, mqsR 3 , pheT,
relE 3 , srlB 2 , srlE 2
ydaL 3 , yfhJ, ygdK
mqsR 3 , pheT, rplC, rplD, rpsA, rpsJ, yhbC, relE 3
fabD, lacI, srlA 2 , srlB 2 , srlD 2 , srlE 2 , sucA 2 , ycjM
ahpC 3 , nrfA 2 , srlD 2 , sucA 2 , torZ, ygjR
Identification of new RNase III targets regulated by YmdB
Relative abundance of RNase III-dependent or -independent transcripts by different level of YmdB or RNase III
RNase III-dependent genes
3.06 ± 0.04
7.37 ± 0.03
39.80 ± 0.01
0.84 ± 0.01
3.27 ± 0.36
8.02 ± 0.02
2.98 ± 0.01
2.86 ± 0.31
21.37 ± 0.01
0.90 ± 0.02
3.34 ± 0.33
7.72 ± 0.01
1.90 ± 0.01
2.37 ± 0.20
3.93 ± 0.01
RNase III-independent genes
qPCR- Δ ymdB 2
qPCR- rnc14 4
0.88 ± 0.13
1.53 ± 0.01
1.36 ± 0.01
0.78 ± 0.01
1.50 ± 0.01
1.15 ± 0.01
0.82 ± 0.01
2.45 ± 0.06
1.86 ± 0.02
1.01 ± 0.01
1.59 ± 0.02
1.38 ± 0.02
0.67 ± 0.01
3.73 ± 0.01
3.30 ± 0.01
Identification of YmdB as a protein that inhibits biofilm formation
RNase III does not affect biofilm inhibition by YmdB
RpoS is required for the inhibition of biofilm formation by YmdB
Both YmdB and RpoS interdependently regulate gene expression and activity on biofilm formation
The 5′ UTR of rpoS mRNA is a known target of RNase III and its levels increase when RNase III activity is ablated . Because biofilm formation is influenced by RpoS levels, it may be proposed that the rpoS mRNA is responsive to YmdB-directed RNase III inhibition. However, this is not the case because the decrease in biofilm formation following YmdB expression was not reversed in the absence of RNase III (Figure 2), suggesting that regulation of RNase III activity by YmdB is not essential for the inhibition of biofilm formation. Thus, the major mechanism underlying biofilm regulation by YmdB appears to be RNase III-independent (Figure 5).
A screen of potential regulatory gene(s) with a YmdB-mediated phenotype demonstrated that RpoS is necessary for inhibiting biofilm formation (Figure 3); RpoS activates the transcription of ymdB; thus, it is highly plausible that the RpoS gene is an upstream regulator of YmdB transcription and the resultant phenotypes. Conversely, the possibility that YmdB is a transcription factor that activates rpoS transcription was initially suggested by observations that RpoS levels were increased by YmdB overexpression, and that YmdB and RpoS are both required for the decrease in biofilm formation. However, this theory was rejected because increases in YmdB expression had no effect on promoter activity (data not shown). Hence, YmdB-induced modulation of RpoS levels must occur via post-transcriptional regulation (Figure 4). It is also possible that YmdB modulates other rpoS transcription factor(s), although we have not identified which other transcription factors are required for this response. Overall, the data suggest that YmdB and RpoS are co-regulators of biofilm formation (Figure 5).
The identification of a novel role for YmdB is not altogether surprising, since eukaryotic macrodomain proteins can have multiple roles [43, 44], and YmdB has additional functions in bacteria [45, 46]. For instance, in E. coli YmdB deacetylates the sirtuin product of O-acetyl-ADP-ribose and reforms ADP ribose . The present study reveals that YmdB modulates the expression of genes involved in physiologically important pathways (Table 1); hence, YmdB could act as a general regulator in a variety of cellular processes. Further examination of such a potential role for YmdB and its family members in bacteria is necessary. YmdB is also required to be coexpressed for the complementation of a function of ClsC, a recently identified cardiolipin synthase in E. coli. ClsC utilizes phosphatidylethanolamines (PE) as the phosphatidyl donor to phosphatidylglycine (PG) to form cardiolipin (CL) . While YmdB is apparently not a direct modulator of that pathway (since changes in clsC (ymdC) gene expression in the microarrays were negligible (a 1.1-fold increase only); (data not shown), it may modulate it indirectly via the action of the fatty acid biosynthesis gene, fabD (Table 1), on the CL synthesis-regulating gene; however, such a role has not been confirmed.
The ectopic expression of YmdB almost completely regulates RNase III activity with respect to several targets, including pnp, rnc and ribosomal RNA processing (Additional file 1: Figure S2) ; however, biofilm formation is not solely dependent upon YmdB-directed RNase III regulation, suggesting that gene expression data will be useful for identifying unknown RNase III-independently regulated YmdB functions.
Several trans-acting factors that modulate the RNase activity of both exo- and endo-RNases have been identified in E. coli[15–18, 47, 48]. Among these four trans-acting regulatory proteins for endo-RNase activity have been well characterized in E. coli: RraA  and RraB  for RNase E, and bacteriophage T7 protein kinase  and YmdB  for RNase III. The presence of homologs in other species suggests such regulation of endo-RNase activity is generally required for bacterial physiology. Recently, gene expression profiling revealed a role for RraA in regulating the SOS response, a mechanism which responds to the stress caused by DNA damage [15, 49]. RNase III modulates approximately 12% (592 genes) of the E. coli genome ; using YmdB-mediated down-regulation of RNase III rather than an RNase III mutant retains the ability to measure the effect of trans-acting factor(s) and hence the correct physiological modulation of RNase III. Because YmdB regulates the turnover of approximately 30% of the target genes of RNase III (Additional file 1: Table S3) and the rpoS level is not completely regulated by YmdB (Figure 4), either other regulator(s) that result RNase III mutant-like conditions must be present or YmdB partially regulates the physiology of the RNase III-mutant to induce the up-regulation of an RNase III activator that has yet to be identified.
The data presented herein show that YmdB functions both to regulate RNase III activity and to modulate bacterial biofilm formation; therefore, YmdB seems to be a multifunctional bacterial macrodomain protein, similar to that in eukaryotic cells. Furthermore, this protein will make it possible to design a more intelligent synthetic scaffold for producing bacterial cells that modulate difficult-to-treat pathogens that depend upon biofilm production.
Availability of supporting data
The data sets supporting the results of this article are included within the article and in Additional file 1.
We thank Dr. Susan Gottesman for distributing RpoS fusion strain (SG30013). This work is supported by the Basic Science Research program through the NRF Korea (2010–0023011) to K.S.K. and the KRIBB initiative program.
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