SR1—a small RNA with two remarkably conserved functions

SR1 is a dual-function sRNA that acts as a base-pairing regulatory RNA on the ahrC mRNA and as a peptide-encoding mRNA on the gapA operon. The SR1-encoded peptide SR1P binds GapA thereby stabilizing gapA mRNA. Under glycolytic conditions, SR1 transcription is repressed by CcpN and CcpA. A computer-based search identified 23 SR1 homologues in Bacillus, Geobacillus, Anoxybacillus and Brevibacillus species. All homologues share a high structural identity with Bacillus subtilis SR1, and the encoded SR1P peptides are highly similar. In the Bacillus cereus group, the sr1p region is present in triplicate or duplicate resulting in longer SR1 species. In all cases, sr1 expression is under control of CcpN, and transcriptional lacZ fusions of nine examined SR1 homologues were sensitive to glucose. Two homologues showed an additional glucose-independent repression by CcpN and an unknown factor. A total of 10 out of 11 tested SR1P homologues complemented a B. subtilis Δsr1 strain in their ability to stabilize gapA mRNA, but only five of them bound GapA tightly. In vitro binding assays with six SR1/ahrC pairs suggest that—despite divergent primary sequences—the base-pairing function is also preserved. In summary, SR1 is an sRNA with two functions that have been conserved over ≈1 billion years.

[1]  F. Kawamura,et al.  Construction of a Bacillus subtilis double mutant deficient in extracellular alkaline and neutral proteases , 1984, Journal of bacteriology.

[2]  S. Brantl.  The copR gene product of plasmid p1P501 acts as a transcriptional repressor at the essential repR promoter , 1994, Molecular microbiology.

[3]  S. Arvidson,et al.  Activation of alpha‐toxin translation in Staphylococcus aureus by the trans‐encoded antisense RNA, RNAIII. , 1995, The EMBO journal.

[4]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[5]  W. Hillen,et al.  Regulation of carbon catabolism in Bacillus species. , 2000, Annual review of microbiology.

[6]  K. Katoh,et al.  MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. , 2002, Nucleic acids research.

[7]  H. Hayashi,et al.  Clostridial VirR/VirS regulon involves a regulatory RNA molecule for expression of toxins , 2002, Molecular microbiology.

[8]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[9]  E. Charpentier,et al.  Synthesis of group A streptococcal virulence factors is controlled by a regulatory RNA molecule , 2004, Molecular microbiology.

[10]  S. Hedges,et al.  A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land , 2004, BMC Evolutionary Biology.

[11]  S. Brantl,et al.  Implication of CcpN in the regulation of a novel untranslated RNA (SR1) in Bacillus subtilis , 2005, Molecular microbiology.

[12]  S. Aymerich,et al.  CcpN (YqzB), a novel regulator for CcpA‐independent catabolite repression of Bacillus subtilis gluconeogenic genes , 2005, Molecular microbiology.

[13]  U. Gerth,et al.  The small untranslated RNA SR1 from the Bacillus subtilis genome is involved in the regulation of arginine catabolism , 2006, Molecular microbiology.

[14]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[15]  June R. Scott,et al.  RivR and the small RNA RivX: the missing links between the CovR regulatory cascade and the Mga regulon , 2007, Molecular microbiology.

[16]  F. Vandenesch,et al.  Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. , 2007, Genes & development.

[17]  J. Vogel,et al.  A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. , 2007, Genes & development.

[18]  I. Moll,et al.  In vitro analysis of the interaction between the small RNA SR1 and its primary target ahrC mRNA , 2007, Nucleic acids research.

[19]  S. Brantl.  Regulatory mechanisms employed by cis-encoded antisense RNAs. , 2007, Current opinion in microbiology.

[20]  C. K. Vanderpool,et al.  A dual function for a bacterial small RNA: SgrS performs base pairing-dependent regulation and encodes a functional polypeptide , 2007, Proceedings of the National Academy of Sciences.

[21]  R. Golbik,et al.  Identification of ligands affecting the activity of the transcriptional repressor CcpN from Bacillus subtilis. , 2008, Journal of molecular biology.

[22]  S. Brantl,et al.  Search for additional targets of the transcriptional regulator CcpN from Bacillus subtilis. , 2009, FEMS microbiology letters.

[23]  M. Vergassola,et al.  The Listeria transcriptional landscape from saprophytism to virulence , 2009, Nature.

[24]  Richard S. P. Horler,et al.  Homologs of the small RNA SgrS are broadly distributed in enteric bacteria but have diverged in size and sequence , 2009, Nucleic acids research.

[25]  S. Rasmussen,et al.  The transcriptionally active regions in the genome of Bacillus subtilis , 2009, Molecular microbiology.

[26]  C. K. Vanderpool,et al.  Characterization of homologs of the small RNA SgrS reveals diversity in function , 2009, Nucleic acids research.

[27]  J. Vogel,et al.  Photooxidative stress‐induced and abundant small RNAs in Rhodobacter sphaeroides , 2009, Molecular microbiology.

[28]  S. Brantl,et al.  The Transcriptional Repressor CcpN from Bacillus subtilis Uses Different Repression Mechanisms at Different Promoters* , 2009, The Journal of Biological Chemistry.

[29]  S. Brantl.  Bacterial chromosome-encoded small regulatory RNAs. , 2009, Future microbiology.

[30]  P. François,et al.  A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation , 2009, Nucleic acids research.

[31]  D. Gautheret,et al.  Experimental discovery of small RNAs in Staphylococcus aureus reveals a riboregulator of central metabolism , 2010, Nucleic acids research.

[32]  V. DiRita,et al.  The Vibrio cholerae virulence regulatory cascade controls glucose uptake through activation of TarA, a small regulatory RNA , 2010, Molecular microbiology.

[33]  J. Vogel,et al.  Identification of regulatory RNAs in Bacillus subtilis , 2010, Nucleic acids research.

[34]  Ulrike Mäder,et al.  A dual‐function sRNA from B. subtilis: SR1 acts as a peptide encoding mRNA on the gapA operon , 2010, Molecular microbiology.

[35]  Rolf Backofen,et al.  The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal , 2011, Molecular microbiology.

[36]  G. Storz,et al.  Bacterial small RNA regulators: versatile roles and rapidly evolving variations. , 2011, Cold Spring Harbor perspectives in biology.

[37]  B. Görke,et al.  Common and divergent features in transcriptional control of the homologous small RNAs GlmY and GlmZ in Enterobacteriaceae , 2010, Nucleic acids research.

[38]  J. Vogel,et al.  The ancestral SgrS RNA discriminates horizontally acquired Salmonella mRNAs through a single G-U wobble pair , 2012, Proceedings of the National Academy of Sciences.