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sRNA EsrE Is Transcriptionally Regulated by the Ferric Uptake Regulator Fur in Escherichia coli

  • Hou, Bingbing (State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology) ;
  • Yang, Xichen (State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology) ;
  • Xia, Hui (State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology) ;
  • Wu, Haizhen (State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology) ;
  • Ye, Jiang (State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology) ;
  • Zhang, Huizhan (State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology)
  • Received : 2019.07.11
  • Accepted : 2019.10.25
  • Published : 2020.01.28

Abstract

Small RNAs (sRNAs) are widespread and play major roles in regulation circuits in bacteria. Previously, we have demonstrated that transcription of esrE is under the control of its own promoter. However, the regulatory elements involved in EsrE sRNA expression are still unknown. In this study, we found that different cis-regulatory elements exist in the promoter region of esrE. We then screened and analyzed seven potential corresponding trans-regulatory elements by using pull-down assays based on DNA affinity chromatography. Among these candidate regulators, we investigated the relationship between the ferric uptake regulator (Fur) and the EsrE sRNA. Electrophoresis mobility shift assays (EMSAs) and β-galactosidase activity assays demonstrated that Fur can bind to the promoter region of esrE, and positively regulate EsrE sRNA expression in the presence of Fe2+.

Keywords

References

  1. Wagner EGH,Romby P. 2015. Small RNAs in bacteria and archaea: who they are, what they do, and how they do it. Adv. Genet. 90: 133-208. https://doi.org/10.1016/bs.adgen.2015.05.001
  2. Melamed S, Peer A, Faigenbaum-Romm R, Gatt YE, Reiss N, Bar A, et al. 2016. Global mapping of small RNA-target interactions in bacteria. Mol. Cell. 63: 884-897. https://doi.org/10.1016/j.molcel.2016.07.026
  3. Frohlich KS, Gottesman S. 2018. Small regulatory RNAs in the enterobacterial response to envelope damage and oxidative stress. Microbiol. Spectr. 6: RWR-0022-2018.
  4. Kavita K, de Mets F, Gottesman S. 2018. New aspects of RNA-based regulation by Hfq and its partner sRNAs. Curr. Opin. Microbiol. 42: 53-61. https://doi.org/10.1016/j.mib.2017.10.014
  5. Gimpel M, Brantl S. 2016. Dual-function sRNA encoded peptide SR1P modulates moonlighting activity of B. subtilis GapA. RNA Biol. 13: 916-926. https://doi.org/10.1080/15476286.2016.1208894
  6. Evguenieva-Hackenberg E, Klug G. 2011. New aspects of RNA processing in prokaryotes. Curr. Opin. Microbiol. 14: 587-592. https://doi.org/10.1016/j.mib.2011.07.025
  7. Klein G, Raina S. 2017. Small regulatory bacterial RNAs regulating the envelope stress response. Biochem. Soc. Trans. 45: 417-425. https://doi.org/10.1042/BST20160367
  8. Klein G, Stupak A, Biernacka D, Wojtkiewicz P, Lindner B, Raina S. 2016. Multiple transcriptional factors regulate transcription of the rpoE gene in Escherichia coli under different growth conditions and when the lipopolysaccharide biosynthesis is defective. J. Biol. Chem. 291: 22999-23019. https://doi.org/10.1074/jbc.M116.748954
  9. Zhang Y, Yan D, Xia L, Zhao X, Osei-Adjei G, Xu S, et al. 2017. The malS-5'UTR regulates hisG, a key gene in the histidine biosynthetic pathway in Salmonella enterica serovar Typhi. Can. J. Microbiol. 63: 287-295. https://doi.org/10.1139/cjm-2016-0490
  10. Chao Y, Vogel J. 2016. A 3' UTR-derived small RNA provides the regulatory noncoding arm of the inner membrane stress response. Mol. Cell 61: 352-363. https://doi.org/10.1016/j.molcel.2015.12.023
  11. Klein G, Kobylak N, Lindner B, Stupak A, Raina S. 2014. Assembly of lipopolysaccharide in Escherichia coli requires the essential LapB heat shock protein. J. Biol. Chem. 289: 14829-14853. https://doi.org/10.1074/jbc.M113.539494
  12. Zhao X, Liu R, Tang H, Osei-Adjei G, Xu S, Zhang Y, et al. 2018. A 3' UTR-derived non-coding RNA RibS increases expression of cfa and promotes biofilm formation of Salmonella enterica serovar Typhi. Res. Microbiol. 169: 279-288. https://doi.org/10.1016/j.resmic.2018.04.007
  13. Kroger C, Rothhardt JE, Brokatzky D, Felsl A, Kary SC, Heermann R, et al. 2018. The small RNA RssR regulates myoinositol degradation by Salmonella enterica. Sci. Rep. 8: 17739. https://doi.org/10.1038/s41598-018-35784-8
  14. Georg J, Hess WR. 2011. cis-antisense RNA, another level of gene regulation in bacteria. Microbiol. Mol. Biol. Rev. 75: 286-300. https://doi.org/10.1128/MMBR.00032-10
  15. Georg J, Hess WR. 2018. Widespread antisense transcription in prokaryotes. Microbiol. Spectr. 6: RWR-0029-2018.
  16. Manna AC, Kim S, Cengher L, Corvaglia A, Leo S, Francois P, et al. 2018. Small RNA teg49 is derived from a sarA transcript and regulates virulence genes independent of SarA in Staphylococcus aureus. Infect. Immun. 86: pii: e00635-17.
  17. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, et al. 2001. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr. Biol. 11: 941-950. https://doi.org/10.1016/S0960-9822(01)00270-6
  18. Saito S, Kakeshita H, Nakamura K. 2009. Novel small RNAencoding genes in the intergenic regions of Bacillus subtilis. Gene 428: 2-8. https://doi.org/10.1016/j.gene.2008.09.024
  19. Baekkedal C, Haugen P. 2015. The Spot 42 RNA: a regulatory small RNA with roles in the central metabolism. RNA Biol. 12: 1071-1077. https://doi.org/10.1080/15476286.2015.1086867
  20. Guo MS, Updegrove TB, Gogol EB, Shabalina SA, Gross CA, Storz G. 2014. MicL, a new ${\sigma}E$-dependent sRNA, combats envelope stress by repressing synthesis of Lpp, the major outer membrane lipoprotein. Genes Dev. 28: 1620-1634. https://doi.org/10.1101/gad.243485.114
  21. Beisel CL, Storz G. 2010. Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol. Rev. 34: 866-882. https://doi.org/10.1111/j.1574-6976.2010.00241.x
  22. Mandin P, Chareyre S, Barras F. 2016. A regulatory circuit composed of a transcription factor, IscR, and a regulatory RNA, RyhB, controls Fe-S cluster delivery. MBio. 7: e00966-16.
  23. Prevost K, Salvail H, Desnoyers G, Jacques JF, Phaneuf E, Masse E. 2007. The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis. Mol. Microbiol. 64: 1260-1273. https://doi.org/10.1111/j.1365-2958.2007.05733.x
  24. Vecerek B, Moll I, Blasi U. 2007. Control of Fur synthesis by the non-coding RNA RyhB and iron-responsive decoding. EMBO J. 26: 965-975. https://doi.org/10.1038/sj.emboj.7601553
  25. Kim HM, Shin JH, Cho YB, Roe JH. 2014. Inverse regulation of Fe- and Ni-containing SOD genes by a Fur family regulator Nur through small RNA processed from 3'UTR of the sodF mRNA. Nucleic Acids Res. 42: 2003-2014. https://doi.org/10.1093/nar/gkt1071
  26. Tanwer P, Bauer S, Heinrichs E, Panda G, Saluja D, Rudel T, Beier D. 2017. Post-transcriptional regulation of target genes by the sRNA FnrS in Neisseria gonorrhoeae. Microbiology 163: 1081-1092. https://doi.org/10.1099/mic.0.000484
  27. Durand S, Storz G. 2010. Reprogramming of anaerobic metabolism by the FnrS small RNA. Mol. Microbiol. 75: 1215-1231. https://doi.org/10.1111/j.1365-2958.2010.07044.x
  28. Chen Z, Wang Y, Li Y, Li Y, Fu N, Ye J, et al. 2012. Esre: a novel essential non-coding RNA in Escherichia coli. FEBS Lett. 586: 1195-1200. https://doi.org/10.1016/j.febslet.2012.03.010
  29. Xia H, Yang X, Tang Q, Ye J, Wu H, Zhang H. 2017. EsrE-a yigP locus-encoded transcript-is a 3' UTR sRNA involved in the respiratory chain of E. coli. Front. Microbiol. 8: 1658. https://doi.org/10.3389/fmicb.2017.01658
  30. Peschke U, Schmidt H, Zhang HZ, Piepersberg W. 1995. Molecular characterization of the lincomycin-production gene cluster of Streptomyces lincolnensis 78-11. Mol. Microbiol. 16: 1137-1156. https://doi.org/10.1111/j.1365-2958.1995.tb02338.x
  31. Wang Y, Ye J, Zhang H. 2012. Identification of transcriptional regulatory sequences of yigP gene in Escherichia coli. Wei Sheng Wu Xue Bao 52: 566-572.
  32. Jutras BL, Verma A, Stevenson B. 2012. Identification of novel DNA-binding proteins using DNA-affinity chromatography/pull down. Curr. Protoc. Microbiol. Chapter 1: Unit1F.1.
  33. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254. https://doi.org/10.1006/abio.1976.9999
  34. Hempelmann E, Krafts K. 2017. The mechanism of silver staining of proteins separated by SDS polyacrylamide gel electrophoresis. Biotech. Histochem. 92: 79-85. https://doi.org/10.1080/10520295.2016.1265149
  35. Hou B, Lin Y, Wu H, Guo M, Petkovic H, Tao L, et al. 2018. The novel transcriptional regulator LmbU promotes lincomycin biosynthesis through regulating expression of its target genes in Streptomyces lincolnensis. J. Bacteriol. 200: e00447-17.
  36. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97: 6640-6645. https://doi.org/10.1073/pnas.120163297
  37. Hoopmann MR, Weisbrod CR, Bruce JE. 2010. Improved strategies for rapid identification of chemically cross-linked peptides using protein interaction reporter technology. J. Proteome. Res. 9: 6323-6333. https://doi.org/10.1021/pr100572u
  38. da Silva Neto JF, Braz VS, Italiani VC, Marques MV. 2009. Fur controls iron homeostasis and oxidative stress defense in the oligotrophic alpha-proteobacterium Caulobacter crescentus. Nucleic Acids Res. 37: 4812-4825. https://doi.org/10.1093/nar/gkp509
  39. Fillat MF. 2014. The FUR (ferric uptake regulator) superfamily: diversity and versatility of key transcriptional regulators. Arch. Biochem. Biophys. 546: 41-52. https://doi.org/10.1016/j.abb.2014.01.029
  40. Seo SW, Kim D, Latif H, O'Brien EJ, Szubin R, Palsson BO. 2014. Deciphering Fur transcriptional regulatory network highlights its complex role beyond iron metabolism in Escherichia coli. Nat. Commun. 5: 4910. https://doi.org/10.1038/ncomms5910
  41. Johnson M, Sengupta M, Purves J, Tarrant E, Williams PH, Cockayne A, et al. 2011. Fur is required for the activation of virulence gene expression through the induction of the sae regulatory system in Staphylococcus aureus. Int. J. Med. Microbiol. 301: 44-52. https://doi.org/10.1016/j.ijmm.2010.05.003
  42. Grunenwald CM, Choby JE, Juttukonda LJ, Beavers WN, Weiss A, Torres VJ, et al. 2019. Manganese detoxification by MntE is critical for resistance to oxidative stress and virulence of Staphylococcus aureus. MBio. 10: pii: e02915-18.
  43. Troxell B, Hassan HM. 2013. Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria. Front. Cell Infect.Microbiol. 3: 59.
  44. Masse E, Gottesman S. 2002. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl. Acad. Sci. USA 99: 4620-4625. https://doi.org/10.1073/pnas.032066599
  45. Pannekoek Y, Huis In't Veld R, Schipper K, Bovenkerk S, Kramer G, Speijer D, et al. 2017. Regulation of Neisseria meningitidis cytochrome bc1 components by NrrF, a Furcontrolled small noncoding RNA. FEBS Open Bio. 7: 1302-1315. https://doi.org/10.1002/2211-5463.12266
  46. Chen Z, Lewis KA, Shultzaberger RK, Lyakhov IG, Zheng M, Doan B, et al. 2007. Discovery of Fur binding site clusters in Escherichia coli by information theory models. Nucleic Acids Res. 35: 6762-6777. https://doi.org/10.1093/nar/gkm631