Bacterial small RNA

Bacterial small RNAs (sRNA) are small RNAs produced by bacteria; they are 50- to 500-nucleotide non-coding RNA molecules, highly structured and containing several stem-loops.[1][2] Numerous sRNAs have been identified using both computational analysis and laboratory-based techniques such as Northern blotting, microarrays and RNA-Seq in a number of bacterial species including Escherichia coli, the model pathogen Salmonella, the nitrogen-fixing alpha-proteobacterium Sinorhizobium meliloti, marine cyanobacteria, Francisella tularensis (the causative agent of tularaemia), Streptococcus pyogenes, and the plant pathogen Xanthomonas oryzae pathovar oryzae.[3][4][5][6][7][8][9][10][11][12]

In the 1960s, the abbreviation sRNA was used to refer to "soluble RNA," which is now known as transfer RNA or tRNA (for an example of the abbreviation used in this sense, see.[13])

Origin

Most bacterial sRNAs are encoded by free-standing genes located in the intergenic regions (IGR) between two known genes.[5][6] However, a class of sRNAs are shown to be derived from the 3'-UTR of mRNAs by independent transcription or nucleolytic cleavage.[14]

Function

sRNAs can either bind to protein targets, and modify the function of the bound protein, or bind to mRNA targets and regulate gene expression. Antisense sRNAs can be categorised as cis-encoded sRNAs, where there is an overlap between the antisense sRNA gene and the target gene, and trans-encoded sRNAs, where the antisense sRNA gene is separate from the target gene.[1][15]

House-keeping

Amongst the targets of sRNAs are a number of house-keeping genes. The 6S RNA binds to RNA polymerase and regulates transcription, tmRNA has functions in protein synthesis, including the recycling of stalled ribosomes, 4.5S RNA regulates signal recognition particle (SRP), which is required for the secretion of proteins and RNase P is involved in maturing tRNAs.[16][17]

Stress response

Many sRNAs are involved in stress response regulation.[18] They are expressed under stress conditions such as cold shock, iron depletion, onset of the SOS response and sugar stress.[17] The small RNA nitrogen stress-induced RNA 1 (NsiR1) is produced by Cyanobacteria under conditions of nitrogen deprivation.[19] Cyanobacteria NisR8 and NsiR9 sRNAs could be related to the differentiation of nitrogen-fixing cells (heterocysts).[20]

Regulation of RpoS

The RpoS gene in E. coli encodes sigma 38, a sigma factor which regulates stress response and acts as a transcriptional regulator for many genes involved in cell adaptation. At least three sRNAs, DsrA, RprA and OxyS, regulate the translation of RpoS. DsrA and RprA both activate RpoS translation by base pairing to a region in the leader sequence of the RpoS mRNA and disrupting formation of a hairpin which frees up the ribosome loading site. OxyS inhibits RpoS translation. DsrA levels are increased in response to low temperatures and osmotic stress, and RprA levels are increased in response to osmotic stress and cell-surface stress, therefore increasing RpoS levels in response to these conditions. Levels of OxyS are increased in response to oxidative stress, therefore inhibiting RpoS under these conditions.[17][21][22]

Regulation of outer membrane proteins

The outer membrane of gram negative bacteria acts as a barrier to prevent the entry of toxins into the bacterial cell, and plays a role in the survival of bacterial cells in diverse environments. Outer membrane proteins (OMPs) include porins and adhesins. Numerous sRNAs regulate the expression of OMPs. The porins OmpC and OmpF are responsible for the transport of metabolites and toxins. The expression of OmpC and OmpF is regulated by the sRNAs MicC and MicF in response to stress conditions.[23][24][25] The outer membrane protein OmpA anchors the outer membrane to the murein layer of the periplasmic space. Its expression is downregulated in the stationary phase of cell-growth. In E. coli the sRNA MicA depletes OmpA levels, in Vibrio cholerae the sRNA VrrA represses synthesis of OmpA in response to stress.[23][26]

Virulence

In some bacteria sRNAs regulate virulence genes. In Salmonella, the pathogenicity island encoded InvR RNA represses synthesis of the major outer membrane protein OmpD; another co-activated DapZ sRNA from 3'-UTR represses abundant membrane Opp/Dpp transporters of oligopeptides;[14] and SgrS sRNA regulates the expression of the secreted effector protein SopD.[4] In Staphylococcus aureus, RNAIII regulates a number of genes involved in toxin and enzyme production and cell-surface proteins.[17] The FasX sRNA is the only well-characterized regulatory RNA known to control the regulation of several virulence factors in Streptococcus pyogenes, including both cell-surface associated adhesion proteins as well as secreted factors.[27][28][29][30]

Quorum sensing

In Vibrio species, the Qrr sRNAs and the chaperone protein Hfq are involved in the regulation of quorum sensing. Qrr sRNAs regulate the expression of several mRNAs including the quorum-sensing master regulators LuxR and HapR.[31][32]

mRNA translational control by 3'UTR

Regulation of eukaryotic but not bacterial mRNA by sequences in the 3' untranslated regions has been widely recognised. However, it has been shown that many mRNAs in S. aureus carry 3'UTRs longer than 100 nucleotides, which may potentially have regulatory function.[33] Further investigation of icaR mRNA (mRNA coding for the repressor of the main expolysaccharidic compound of the bacteria biofilm matrix) demonstrated that the 3'UTR binding to the 5' UTR can interfere with the translation initiation complex and generate a double stranded substrate for RNaseIII. Mozos at al. showed that the interaction is between UCCCCUG motif in the 3'UTR and the Shine-Dalagarno region at the 5'UTR. Deletion of the motif resulted in IcaR repressor accumulation and inhibition of biofilm development.

Target prediction

In order to understand an sRNA's function one primarily needs to describe its targets. Here, target predictions represent a sensible, fast and free method for initial characterization of putative targets, given that the sRNA actually exerts its function via direct base pairing with a target RNA. Examples are CopraRNA,[34][35] IntaRNA,[35][36] TargetRNA[37] and RNApredator.[38] It has been shown that target prediction for enterobacterial sRNAs can benefit from transcriptome wide Hfq-binding maps.[39]

Database

BSRD (kwanlab.bio.cuhk.edu.hk/BSRD) is a repository for published sRNA sequences with multiple valuable annotations and expression profiles.[40]

See also

References

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  2. ↑ Viegas SC, Arraiano CM (2008). "Regulating the regulators: How ribonucleases dictate the rules in the control of small non-coding RNAs". RNA Biol. 5 (4): 230–43. doi:10.4161/rna.6915. PMID 18981732.
  3. ↑ Hershberg R, Altuvia S, Margalit H (April 2003). "A survey of small RNA-encoding genes in Escherichia coli". Nucleic Acids Res. 31 (7): 1813–20. doi:10.1093/nar/gkg297. PMC 152812Freely accessible. PMID 12654996.
  4. 1 2 Vogel J (January 2009). "A rough guide to the non-coding RNA world of Salmonella". Mol. Microbiol. 71 (1): 1–11. doi:10.1111/j.1365-2958.2008.06505.x. PMID 19007416.
  5. 1 2 Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S (July 2001). "Identification of novel small RNAs using comparative genomics and microarrays". Genes Dev. 15 (13): 1637–51. doi:10.1101/gad.901001. PMC 312727Freely accessible. PMID 11445539.
  6. 1 2 Argaman L, Hershberg R, Vogel J, et al. (June 2001). "Novel small RNA-encoding genes in the intergenic regions of Escherichia coli". Curr. Biol. 11 (12): 941–50. doi:10.1016/S0960-9822(01)00270-6. PMID 11448770.
  7. ↑ Rivas E, Klein RJ, Jones TA, Eddy SR (September 2001). "Computational identification of noncoding RNAs in E. coli by comparative genomics". Curr. Biol. 11 (17): 1369–73. doi:10.1016/S0960-9822(01)00401-8. PMID 11553332.
  8. ↑ Schlüter JP, Reinkensmeier J, Daschkey S, et al. (2010). "A genome-wide survey of sRNAs in the symbiotic nitrogen-fixing alpha-proteobacterium Sinorhizobium meliloti". BMC Genomics. 11: 245. doi:10.1186/1471-2164-11-245. PMC 2873474Freely accessible. PMID 20398411.
  9. ↑ Axmann IM, Kensche P, Vogel J, Kohl S, Herzel H, Hess WR (2005). "Identification of cyanobacterial non-coding RNAs by comparative genome analysis". Genome Biol. 6 (9): R73. doi:10.1186/gb-2005-6-9-r73. PMC 1242208Freely accessible. PMID 16168080.
  10. ↑ Postic G, Frapy E, Dupuis M, et al. (2010). "Identification of small RNAs in Francisella tularensis". BMC Genomics. 11: 625. doi:10.1186/1471-2164-11-625. PMC 3091763Freely accessible. PMID 21067590.
  11. ↑ Liang H, Zhao YT, Zhang JQ, Wang XJ, Fang RX, Jia YT (2011). "Identification and functional characterization of small non-coding RNAs in Xanthomonas oryzae pathovar oryzae". BMC Genomics. 12: 87. doi:10.1186/1471-2164-12-87. PMC 3039613Freely accessible. PMID 21276262.
  12. ↑ Tesorero, Rafael A.; Yu, Ning; Wright, Jordan O.; Svencionis, Juan P.; Cheng, Qiang; Kim, Jeong-Ho; Cho, Kyu Hong (2013-01-01). "Novel regulatory small RNAs in Streptococcus pyogenes". PloS One. 8 (6): e64021. doi:10.1371/journal.pone.0064021. ISSN 1932-6203. PMC 3675131Freely accessible. PMID 23762235.
  13. ↑ Crick F (1966). "Codon–anticodon pairing: the wobble hypothesis" (PDF). J Mol Biol. 19 (2): 548–55. doi:10.1016/S0022-2836(66)80022-0. PMID 5969078.
  14. 1 2 Chao Y, Papenfort K, Reinhardt R, Sharma CM, Vogel J (October 2012). "An atlas of Hfq-bound transcripts reveals 3' UTRs as a genomic reservoir of regulatory small RNAs.". EMBO J. 31 (20): 4005–19. doi:10.1038/emboj.2012.229. PMID 22922465.
  15. ↑ Cao Y, Wu J, Liu Q, et al. (November 2010). "sRNATarBase: a comprehensive database of bacterial sRNA targets verified by experiments". RNA. 16 (11): 2051–7. doi:10.1261/rna.2193110. PMC 2957045Freely accessible. PMID 20843985.
  16. ↑ Wassarman KM (April 2007). "6S RNA: a small RNA regulator of transcription". Curr. Opin. Microbiol. 10 (2): 164–8. doi:10.1016/j.mib.2007.03.008. PMID 17383220.
  17. 1 2 3 4 Christian Hammann; Nellen, Wolfgang (2005). Small RNAs:: Analysis and Regulatory Functions (Nucleic Acids and Molecular Biology). Berlin: Springer. ISBN 3-540-28129-0.
  18. ↑ Caswell CC, Oglesby-Sherrouse AG, Murphy ER (October 2014). "Sibling rivalry: related bacterial small RNAs and their redundant and non-redundant roles". Front Cell Infect Microbiol. 2014 (4): 151. doi:10.3389/fcimb.2014.00151. PMC 4211561Freely accessible. PMID 25389522.
  19. ↑ Ionescu, D; Voss, B; Oren, A; Hess, WR; Muro-Pastor, AM (Apr 30, 2010). "Heterocyst-specific transcription of NsiR1, a non-coding RNA encoded in a tandem array of direct repeats in cyanobacteria.". Journal of Molecular Biology. 398 (2): 177–88. doi:10.1016/j.jmb.2010.03.010. PMID 20227418.
  20. ↑ Brenes-Álvarez, Manuel; Olmedo-Verd, Elvira; Vioque, Agustín; Muro-Pastor, Alicia M. (2016-01-01). "Identification of Conserved and Potentially Regulatory Small RNAs in Heterocystous Cyanobacteria". Frontiers in Microbiology. 7: 48. doi:10.3389/fmicb.2016.00048. ISSN 1664-302X. PMC 4734099Freely accessible. PMID 26870012.
  21. ↑ Repoila F, Majdalani N, Gottesman S (May 2003). "Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm". Mol. Microbiol. 48 (4): 855–61. doi:10.1046/j.1365-2958.2003.03454.x. PMID 12753181.
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  33. ↑ Ruiz de los Mozos, Igor; Vergara-Irigaray, Marta; Segura, Victor; Villanueva, Maite; Bitarte, Nerea; Saramago, Margarida; Domingues, Susana; Arraiano, Cecilia M.; Fechter, Pierre (2013-01-01). "Base pairing interaction between 5'- and 3'-UTRs controls icaR mRNA translation in Staphylococcus aureus". PLoS genetics. 9 (12): e1004001. doi:10.1371/journal.pgen.1004001. ISSN 1553-7404. PMC 3868564Freely accessible. PMID 24367275.
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  35. 1 2 Wright PR, Georg J, Mann M, Sorescu DA, Richter AS, Lott S, Kleinkauf R, Hess WR, Backofen R (2014). "CopraRNA and IntaRNA: predicting small RNA targets, networks and interaction domains.". Nucleic Acids Res. 42 (Web Server): W119–23. doi:10.1093/nar/gku359. PMID 24838564.
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