RyhB

Secondary structure for the RyhB RNA. The Sm-like protein Hfq binds to the AU-rich unstructured region of RyhB as indicated. Below the secondary structure, the primary sequence of RyhB is shown along with its putative binding interaction to the target mRNA sodB. The start codon for sodB is underlined. RyhB nucleotides that participate in the interaction are in bold.[1]

RyhB RNA is a 90 nucleotide RNA that down-regulates a set of iron-storage and iron-using proteins when iron is limiting; it is itself negatively regulated by the ferric uptake repressor protein, Fur (Ferric uptake regulator).

Discovery

The gene was independently identified in two screens, named RyhB by Wassarman et al. and called SraI by Argaman et al. and was found to be expressed only in stationary phase.[2][3]

Function and regulation

RyhB RNA levels are inversely correlated with mRNA levels for the sdhCDAB operon, encoding succinate dehydrogenase, as well as five other genes previously shown to be positively regulated by Fur by an unknown mechanism. These include two other genes encoding enzymes in the tricarboxylic acid cycle, acnA and fumA, two ferritin genes, ftnA and bfr, and a gene for superoxide dismutase, sodB.[4] A number of other genes have been predicted computationally and verified as targets by microarray analysis: napF, sodA, cysE, yciS, acpS, nagZ and dadA.[1] RyhB is bound by the Hfq protein, that increases its interaction with its target messages.

A comparative genomics target prediction approach suggests that the mRNAs of eleven additional iron containing proteins are controlled by RyhB in Escherichia coli. Two of those (erpA, nirB) and two additional targets that are not directly related to iron (nagZ, marA) were verified with a GFP reporter system.[5][6]

It has been shown that RyhB has a role in targeting the polycistronic transcript iscRSUA for differential degradation. RyhB binds to the second cistron of iscRSUA, which encodes machinery for biosynthesis of Fe-S clusters. This binding promotes cleavage of the downstream iscSUA transcript. This cleavage leaves the 5' IscR transcript which is a transcriptional regulator responsible regulating several genes that depend on cellular Fe-S level.[7]

More recent data indicate a potential dual function role for RyhB. In this capacity it may act both as an RNA-RNA interaction based regulator and as a transcript encoding for a small protein.[8]

RyhB is analogous to PrrF RNA found in Pseudomonas aeruginosa,[9] to HrrF RNA in Haemophilus species [10] and to IsaR1 in cyanobacteria.[11][12]

First sRNA shown to mediate persistence to antibiotics in E.coli. The finding may lead to discovery of novel treatments for persistent infections.[13]

Naming

The RyhB gene name is an acronym composed of R for RNA, y for unknown function (after the protein naming convention), with the h representing the ten-minute-interval section of the E. coli map the gene is found in. The B comes from the fact that this was one of two RNA genes identified in this interval.[3] Other RNAs using this nomenclature include RydB RNA, RyeB RNA, RyeE RNA and RyfA RNA.

References

  1. 1 2 Tjaden B, Goodwin SS, Opdyke JA, Guillier M, Fu DX, Gottesman S, Storz G, et al. (2006). "Target prediction for small, noncoding RNAs in bacteria". Nucleic Acids Research. 34 (9): 2791–802. doi:10.1093/nar/gkl356. PMC 1464411. PMID 16717284.
  2. ↑ Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, Altuvia S (June 2001). "Novel small RNA-encoding genes in the intergenic regions of Escherichia coli". Current Biology. 11 (12): 941–50. doi:10.1016/S0960-9822(01)00270-6. PMID 11448770.
  3. 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 & Development. 15 (13): 1637–51. doi:10.1101/gad.901001. PMC 312727. PMID 11445539.
  4. ↑ Massé E, Gottesman S (April 2002). "A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli". Proceedings of the National Academy of Sciences of the United States of America. 99 (7): 4620–5. doi:10.1073/pnas.032066599. PMC 123697. PMID 11917098.
  5. ↑ Wright PR, Richter AS, Papenfort K, Mann M, Vogel J, Hess WR, Backofen R, Georg J (September 2013). "Comparative genomics boosts target prediction for bacterial small RNAs". Proceedings of the National Academy of Sciences of the United States of America. 110 (37): E3487–96. doi:10.1073/pnas.1303248110. PMC 3773804. PMID 23980183.
  6. ↑ Urban JH, Vogel J (2007). "Translational control and target recognition by Escherichia coli small RNAs in vivo". Nucleic Acids Research. 35 (3): 1018–37. doi:10.1093/nar/gkl1040. PMC 1807950. PMID 17264113.
  7. ↑ Desnoyers G, Morissette A, Prévost K, Massé E (June 2009). "Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA". The EMBO Journal. 28 (11): 1551–61. doi:10.1038/emboj.2009.116. PMC 2693151. PMID 19407815.
  8. ↑ Neuhaus K, Landstorfer R, Simon S, Schober S, Wright PR, Smith C, Backofen R, Wecko R, Keim DA, Scherer S (February 2017). "Differentiation of ncRNAs from small mRNAs in Escherichia coli O157:H7 EDL933 (EHEC) by combined RNAseq and RIBOseq - ryhB encodes the regulatory RNA RyhB and a peptide, RyhP". BMC Genomics. 18 (1): 216. doi:10.1186/s12864-017-3586-9. PMC 5331693. PMID 28245801.
  9. ↑ Wilderman PJ, Sowa NA, FitzGerald DJ, FitzGerald PC, Gottesman S, Ochsner UA, Vasil ML (June 2004). "Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis". Proceedings of the National Academy of Sciences of the United States of America. 101 (26): 9792–7. doi:10.1073/pnas.0403423101. PMC 470753. PMID 15210934.
  10. ↑ Santana EA, Harrison A, Zhang X, Baker BD, Kelly BJ, White P, Liu Y, Munson RS (2014-01-01). "HrrF is the Fur-regulated small RNA in nontypeable Haemophilus influenzae". PLOS One. 9 (8): e105644. doi:10.1371/journal.pone.0105644. PMC 4144887. PMID 25157846.
  11. ↑ Georg J, Kostova G, Vuorijoki L, Schön V, Kadowaki T, Huokko T, Baumgartner D, Müller M, Klähn S, Allahverdiyeva Y, Hihara Y, Futschik ME, Aro EM, Hess WR (May 2017). "Acclimation of Oxygenic Photosynthesis to Iron Starvation Is Controlled by the sRNA IsaR1". Current Biology. 27 (10): 1425–1436.e7. doi:10.1016/j.cub.2017.04.010. PMID 28479323.
  12. ↑ Rübsam H, Kirsch F, Reimann V, Erban A, Kopka J, Hagemann M, Hess WR, Klähn S (February 2018). "The iron-stress activated RNA 1 (IsaR1) coordinates osmotic acclimation and iron starvation responses in the cyanobacterium Synechocystis sp. PCC 6803". Environmental Microbiology. doi:10.1111/1462-2920.14079. PMID 29468839.
  13. ↑ Zhang S, Liu S, Wu N, Yuan Y, Zhang W, Zhang Y (2018). "Escherichia coli by Reducing Cellular Metabolism". Frontiers in Microbiology. 9: 136. doi:10.3389/fmicb.2018.00136. PMC 5808207. PMID 29467745.

Further reading

  • Salvail H, Lanthier-Bourbonnais P, Sobota JM, Caza M, Benjamin JA, Mendieta ME, Lépine F, Dozois CM, Imlay J, Massé E (August 2010). "A small RNA promotes siderophore production through transcriptional and metabolic remodeling". Proceedings of the National Academy of Sciences of the United States of America. 107 (34): 15223–8. doi:10.1073/pnas.1007805107. PMC 2930555. PMID 20696910.
  • Nandal A, Huggins CC, Woodhall MR, McHugh J, Rodríguez-Quiñones F, Quail MA, Guest JR, Andrews SC (February 2010). "Induction of the ferritin gene (ftnA) of Escherichia coli by Fe(2+)-Fur is mediated by reversal of H-NS silencing and is RyhB independent". Molecular Microbiology. 75 (3): 637–57. doi:10.1111/j.1365-2958.2009.06977.x. PMID 20015147.
  • Bollinger CJ, Kallio PT (October 2007). "Impact of the small RNA RyhB on growth, physiology and heterologous protein expression in Escherichia coli". FEMS Microbiology Letters. 275 (2): 221–8. doi:10.1111/j.1574-6968.2007.00880.x. PMID 17784860.
  • Prévost K, Salvail H, Desnoyers G, Jacques JF, Phaneuf E, Massé E (June 2007). "The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis". Molecular Microbiology. 64 (5): 1260–73. doi:10.1111/j.1365-2958.2007.05733.x. PMID 17542919.
  • Murphy ER, Payne SM (July 2007). "RyhB, an iron-responsive small RNA molecule, regulates Shigella dysenteriae virulence". Infection and Immunity. 75 (7): 3470–7. doi:10.1128/IAI.00112-07. PMC 1932958. PMID 17438026.
  • Vecerek B, Moll I, Bläsi U (February 2007). "Control of Fur synthesis by the non-coding RNA RyhB and iron-responsive decoding". The EMBO Journal. 26 (4): 965–75. doi:10.1038/sj.emboj.7601553. PMC 1852835. PMID 17268550.
  • Jacques JF, Jang S, Prévost K, Desnoyers G, Desmarais M, Imlay J, Massé E (November 2006). "RyhB small RNA modulates the free intracellular iron pool and is essential for normal growth during iron limitation in Escherichia coli". Molecular Microbiology. 62 (4): 1181–90. doi:10.1111/j.1365-2958.2006.05439.x. PMID 17078818.
  • Oglesby AG, Murphy ER, Iyer VR, Payne SM (December 2005). "Fur regulates acid resistance in Shigella flexneri via RyhB and ydeP". Molecular Microbiology. 58 (5): 1354–67. doi:10.1111/j.1365-2958.2005.04920.x. PMID 16313621.
  • Massé E, Vanderpool CK, Gottesman S (October 2005). "Effect of RyhB small RNA on global iron use in Escherichia coli" (Free full text). Journal of Bacteriology. 187 (20): 6962–71. doi:10.1128/JB.187.20.6962-6971.2005. PMC 1251601. PMID 16199566.
  • Mey AR, Craig SA, Payne SM (September 2005). "Characterization of Vibrio cholerae RyhB: the RyhB regulon and role of ryhB in biofilm formation". Infection and Immunity. 73 (9): 5706–19. doi:10.1128/IAI.73.9.5706-5719.2005. PMC 1231101. PMID 16113288.
  • Davis BM, Quinones M, Pratt J, Ding Y, Waldor MK (June 2005). "Characterization of the small untranslated RNA RyhB and its regulon in Vibrio cholerae". Journal of Bacteriology. 187 (12): 4005–14. doi:10.1128/JB.187.12.4005-4014.2005. PMC 1151736. PMID 15937163.
  • Gottesman S (July 2005). "Micros for microbes: non-coding regulatory RNAs in bacteria". Trends in Genetics. 21 (7): 399–404. doi:10.1016/j.tig.2005.05.008. PMID 15913835.
  • Afonyushkin T, Vecerek B, Moll I, Bläsi U, Kaberdin VR (2005). "Both RNase E and RNase III control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB". Nucleic Acids Research. 33 (5): 1678–89. doi:10.1093/nar/gki313. PMC 1069011. PMID 15781494.
  • Oglesby-Sherrouse AG, Murphy ER (April 2013). "Iron-responsive bacterial small RNAs: variations on a theme". Metallomics. 5 (4): 276–86. doi:10.1039/c3mt20224k. PMC 3612141. PMID 23340911.
  • Tanabe T, Funahashi T, Nakao H, Maki J, Yamamoto S (August 2013). "The Vibrio parahaemolyticus small RNA RyhB promotes production of the siderophore vibrioferrin by stabilizing the polycistronic mRNA". Journal of Bacteriology. 195 (16): 3692–703. doi:10.1128/JB.00162-13. PMC 3754555. PMID 23772063.
  • Bos J, Duverger Y, Thouvenot B, Chiaruttini C, Branlant C, Springer M, Charpentier B, Barras F (2013). Cascales E, ed. "The sRNA RyhB regulates the synthesis of the Escherichia coli methionine sulfoxide reductase MsrB but not MsrA". PLOS One. 8 (5): e63647. doi:10.1371/journal.pone.0063647. PMC 3650055. PMID 23671689.
  • Deng Z, Liu Z, Bi Y, Wang X, Zhou D, Yang R, Han Y (2014). "Rapid degradation of Hfq-free RyhB in Yersinia pestis by PNPase independent of putative ribonucleolytic complexes". BioMed Research International. 2014: 798918. doi:10.1155/2014/798918. PMC 4003864. PMID 24818153.
  • Li F, Wang Y, Gong K, Wang Q, Liang Q, Qi Q (January 2014). "Constitutive expression of RyhB regulates the heme biosynthesis pathway and increases the 5-aminolevulinic acid accumulation in Escherichia coli". FEMS Microbiology Letters. 350 (2): 209–15. doi:10.1111/1574-6968.12322. PMID 24188714.
  • Porcheron G, Habib R, Houle S, Caza M, Lépine F, Daigle F, Massé E, Dozois CM (December 2014). "The small RNA RyhB contributes to siderophore production and virulence of uropathogenic Escherichia coli". Infection and Immunity. 82 (12): 5056–68. doi:10.1128/IAI.02287-14. PMC 4249264. PMID 25245805.
  • Calderón PF, Morales EH, Acuña LG, Fuentes DN, Gil F, Porwollik S, McClelland M, Saavedra CP, Calderón IL (July 2014). "The small RNA RyhB homologs from Salmonella typhimurium participate in the response to S-nitrosoglutathione-induced stress". Biochemical and Biophysical Research Communications. 450 (1): 641–5. doi:10.1016/j.bbrc.2014.06.031. PMID 24937451.
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