1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

EcoSal Plus

Domain 4:

Synthesis and Processing of Macromolecules

Trans-Acting Small RNAs and Their Effects on Gene Expression in and

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • PDF
    10.79 MB
  • XML
    206.11 Kb
  • HTML
    199.80 Kb
  • Authors: Jens Hör1, Gianluca Matera2, Jörg Vogel3,4, Susan Gottesman5, and Gisela Storz6
  • Editors: Susan T. Lovett7, Deborah Hinton8
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institute of Molecular Infection Biology, University of Würzburg, 97080 Würzburg, Germany; 2: Institute of Molecular Infection Biology, University of Würzburg, 97080 Würzburg, Germany; 3: Institute of Molecular Infection Biology, University of Würzburg, 97080 Würzburg, Germany; 4: Helmholtz Institute for RNA-based Infection Research (HIRI), 97080 Würzburg, Germany; 5: Laboratory of Molecular Biology, National Cancer Institute, Bethesda, MD 20892; 6: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892; 7: Brandeis University, Waltham, MA; 8: Laboratory of Cell and Molecular Biology, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, MD
  • Received 23 November 2019 Accepted 03 January 2020 Published 20 March 2020
  • Address correspondence to Jörg Vogel, [email protected]; Susan Gottesman, [email protected]; Gisela Storz, [email protected]
image of Trans-Acting Small RNAs and Their Effects on Gene Expression in <span class="jp-italic">Escherichia coli</span> and <span class="jp-italic">Salmonella enterica</span>
    Preview this reference work article:
    Preview Magnify
    Zoom in
    Zoomout

    Trans-Acting Small RNAs and Their Effects on Gene Expression in and , Page 1 of 2

    | /docserver/preview/fulltext/ecosalplus/9/1/ESP-0030-2019-1.gif /docserver/preview/fulltext/ecosalplus/9/1/ESP-0030-2019-2.gif

  • Abstract:

    The last few decades have led to an explosion in our understanding of the major roles that small regulatory RNAs (sRNAs) play in regulatory circuits and the responses to stress in many bacterial species. Much of the foundational work was carried out with and serovar Typhimurium. The studies of these organisms provided an overview of how the sRNAs function and their impact on bacterial physiology, serving as a blueprint for sRNA biology in many other prokaryotes. They also led to the development of new technologies. In this chapter, we first summarize how these sRNAs were identified, defining them in the process. We discuss how they are regulated and how they act and provide selected examples of their roles in regulatory circuits and the consequences of this regulation. Throughout, we summarize the methodologies that were developed to identify and study the regulatory RNAs, most of which are applicable to other bacteria. Newly updated databases of the known sRNAs in K-12 and Typhimurium SL1344 serve as a reference point for much of the discussion and, hopefully, as a resource for readers and for future experiments to address open questions raised in this review.

  • Citation: Hör J, Matera G, Vogel J, Gottesman S, Storz G. 2020. Trans-Acting Small RNAs and Their Effects on Gene Expression in and , EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0030-2019

References

1. Wassarman KM, Zhang A, Storz G. 1999. Small RNAs in Escherichia coli. Trends Microbiol 7:37–45 http://dx.doi.org/10.1016/S0966-842X(98)01379-1.
2. Inouye M, Delihas N. 1988. Small RNAs in the prokaryotes: a growing list of diverse roles. Cell 53:5–7 http://dx.doi.org/10.1016/0092-8674(88)90480-1.
3. Eguchi Y, Itoh T, Tomizawa J. 1991. Antisense RNA. Annu Rev Biochem 60:631–652 http://dx.doi.org/10.1146/annurev.bi.60.070191.003215. [PubMed]
4. Wagner EGH, Simons RW. 1994. Antisense RNA control in bacteria, phages, and plasmids. Annu Rev Microbiol 48:713–742 http://dx.doi.org/10.1146/annurev.mi.48.100194.003433. [PubMed]
5. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM, et al. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512 http://dx.doi.org/10.1126/science.7542800. [PubMed]
6. Blattner FR, Plunkett G III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462 http://dx.doi.org/10.1126/science.277.5331.1453.
7. Cech TR, Steitz JA. 2014. The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157:77–94 http://dx.doi.org/10.1016/j.cell.2014.03.008. [PubMed]
8. Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S. 2001. Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev 15:1637–1651 http://dx.doi.org/10.1101/gad.901001. [PubMed]
9. Chen S, Lesnik EA, Hall TA, Sampath R, Griffey RH, Ecker DJ, Blyn LB. 2002. A bioinformatics based approach to discover small RNA genes in the Escherichia coli genome. Biosystems 65:157–177 http://dx.doi.org/10.1016/S0303-2647(02)00013-8.
10. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EGH, Margalit H, Altuvia S. 2001. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 11:941–950 http://dx.doi.org/10.1016/S0960-9822(01)00270-6.
11. Kawano M, Reynolds AA, Miranda-Rios J, Storz G. 2005. Detection of 5′- and 3′-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli. Nucleic Acids Res 33:1040–1050 http://dx.doi.org/10.1093/nar/gki256. [PubMed]
12. Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jäger JG, Hüttenhofer A, Wagner EGH. 2003. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 31:6435–6443 http://dx.doi.org/10.1093/nar/gkg867. [PubMed]
13. Kröger C, Dillon SC, Cameron AD, Papenfort K, Sivasankaran SK, Hokamp K, Chao Y, Sittka A, Hébrard M, Händler K, Colgan A, Leekitcharoenphon P, Langridge GC, Lohan AJ, Loftus B, Lucchini S, Ussery DW, Dorman CJ, Thomson NR, Vogel J, Hinton JC. 2012. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci USA 109:E1277–E1286 http://dx.doi.org/10.1073/pnas.1201061109. [PubMed]
14. Thomason MK, Bischler T, Eisenbart SK, Förstner KU, Zhang A, Herbig A, Nieselt K, Sharma CM, Storz G. 2015. Global transcriptional start site mapping using differential RNA sequencing reveals novel antisense RNAs in Escherichia coli. J Bacteriol 197:18–28 http://dx.doi.org/10.1128/JB.02096-14. [PubMed]
15. Zhang A, Altuvia S, Tiwari A, Argaman L, Hengge-Aronis R, Storz G. 1998. The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J 17:6061–6068 http://dx.doi.org/10.1093/emboj/17.20.6061. [PubMed]
16. Sledjeski DD, Whitman C, Zhang A. 2001. Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 183:1997–2005 http://dx.doi.org/10.1128/JB.183.6.1997-2005.2001. [PubMed]
17. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, Gottesman S. 2003. Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 50:1111–1124 http://dx.doi.org/10.1046/j.1365-2958.2003.03734.x. [PubMed]
18. Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, Hinton JC, Vogel J. 2008. Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 4:e1000163 http://dx.doi.org/10.1371/journal.pgen.1000163. [PubMed]
19. Chao Y, Papenfort K, Reinhardt R, Sharma CM, Vogel J. 2012. An atlas of Hfq-bound transcripts reveals 3′ UTRs as a genomic reservoir of regulatory small RNAs. EMBO J 31:4005–4019 http://dx.doi.org/10.1038/emboj.2012.229. [PubMed]
20. Melamed S, Peer A, Faigenbaum-Romm R, Gatt YE, Reiss N, Bar A, Altuvia Y, Argaman L, Margalit H. 2016. Global mapping of small RNA-target interactions in bacteria. Mol Cell 63:884–897 http://dx.doi.org/10.1016/j.molcel.2016.07.026. [PubMed]
21. Tree JJ, Granneman S, McAteer SP, Tollervey D, Gally DL. 2014. Identification of bacteriophage-encoded anti-sRNAs in pathogenic Escherichia coli. Mol Cell 55:199–213 http://dx.doi.org/10.1016/j.molcel.2014.05.006. [PubMed]
22. Holmqvist E, Wright PR, Li L, Bischler T, Barquist L, Reinhardt R, Backofen R, Vogel J. 2016. Global RNA recognition patterns of post-transcriptional regulators Hfq and CsrA revealed by UV crosslinking in vivo. EMBO J 35:991–1011 http://dx.doi.org/10.15252/embj.201593360. [PubMed]
23. Holmqvist E, Li L, Bischler T, Barquist L, Vogel J. 2018. Global maps of ProQ binding in vivo reveal target recognition via RNA structure and stability control at mRNA 3′ ends. Mol Cell 70:971–982.e6 http://dx.doi.org/10.1016/j.molcel.2018.04.017. [PubMed]
24. Potts AH, Vakulskas CA, Pannuri A, Yakhnin H, Babitzke P, Romeo T. 2017. Global role of the bacterial post-transcriptional regulator CsrA revealed by integrated transcriptomics. Nat Commun 8:1596 http://dx.doi.org/10.1038/s41467-017-01613-1. [PubMed]
25. Melamed S, Adams PP, Zhang A, Zhang H, Storz G. 2020. RNA-RNA interactomes of ProQ and Hfq reveal overlapping and competing roles. Mol Cell 77:411–425.e7 http://dx.doi.org/10.1016/j.molcel.2019.10.022. [PubMed]
26. Smirnov A, Förstner KU, Holmqvist E, Otto A, Günster R, Becher D, Reinhardt R, Vogel J. 2016. Grad-seq guides the discovery of ProQ as a major small RNA-binding protein. Proc Natl Acad Sci USA 113:11591–11596 http://dx.doi.org/10.1073/pnas.1609981113. [PubMed]
27. Queiroz RML, Smith T, Villanueva E, Marti-Solano M, Monti M, Pizzinga M, Mirea DM, Ramakrishna M, Harvey RF, Dezi V, Thomas GH, Willis AE, Lilley KS. 2019. Comprehensive identification of RNA-protein interactions in any organism using orthogonal organic phase separation (OOPS). Nat Biotechnol 37:169–178 http://dx.doi.org/10.1038/s41587-018-0001-2. [PubMed]
28. Shchepachev V, Bresson S, Spanos C, Petfalski E, Fischer L, Rappsilber J, Tollervey D. 2019. Defining the RNA interactome by total RNA-associated protein purification. Mol Syst Biol 15:e8689 http://dx.doi.org/10.15252/msb.20188689. [PubMed]
29. Urdaneta EC, Vieira-Vieira CH, Hick T, Wessels HH, Figini D, Moschall R, Medenbach J, Ohler U, Granneman S, Selbach M, Beckmann BM. 2019. Purification of cross-linked RNA-protein complexes by phenol-toluol extraction. Nat Commun 10:990 http://dx.doi.org/10.1038/s41467-019-08942-3. [PubMed]
30. Bhatt S, Egan M, Jenkins V, Muche S, El-Fenej J. 2016. The tip of the iceberg: on the roles of regulatory small RNAs in the virulence of enterohemorrhagic and enteropathogenic Escherichia coli. Front Cell Infect Microbiol 6:105 http://dx.doi.org/10.3389/fcimb.2016.00105. [PubMed]
31. Padalon-Brauch G, Hershberg R, Elgrably-Weiss M, Baruch K, Rosenshine I, Margalit H, Altuvia S. 2008. Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res 36:1913–1927 http://dx.doi.org/10.1093/nar/gkn050. [PubMed]
32. Pfeiffer V, Sittka A, Tomer R, Tedin K, Brinkmann V, Vogel J. 2007. A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome. Mol Microbiol 66:1174–1191 http://dx.doi.org/10.1111/j.1365-2958.2007.05991.x. [PubMed]
33. Kröger C, Colgan A, Srikumar S, Händler K, Sivasankaran SK, Hammarlöf DL, Canals R, Grissom JE, Conway T, Hokamp K, Hinton JC. 2013. An infection-relevant transcriptomic compendium for Salmonella enterica serovar Typhimurium. Cell Host Microbe 14:683–695 http://dx.doi.org/10.1016/j.chom.2013.11.010. [PubMed]
34. Sharma CM, Papenfort K, Pernitzsch SR, Mollenkopf HJ, Hinton JC, Vogel J. 2011. Pervasive post-transcriptional control of genes involved in amino acid metabolism by the Hfq-dependent GcvB small RNA. Mol Microbiol 81:1144–1165 http://dx.doi.org/10.1111/j.1365-2958.2011.07751.x. [PubMed]
35. Ellermeier JR, Slauch JM. 2008. Fur regulates expression of the Salmonella pathogenicity island 1 type III secretion system through HilD. J Bacteriol 190:476–486 http://dx.doi.org/10.1128/JB.00926-07. [PubMed]
36. Karp PD, Ong WK, Paley S, Billington R, Caspi R, Fulcher C, Kothari A, Krummenacker M, Latendresse M, Midford PE, Subhraveti P, Gama-Castro S, Muñiz-Rascado L, Bonavides-Martinez C, Santos-Zavaleta A, Mackie A, Collado-Vides J, Keseler IM, Paulsen I. 12 November 2018, posting date. The EcoCyc Database. Ecosal Plus 2015 10.1128/ecosalplus.ESP-0006-2018. http://dx.doi.org/10.1128/ecosalplus.ESP-0006-2018. [PubMed]
37. Georg J, Hess WR. 2018. Widespread antisense transcription in prokaryotes. Microbiol Spectr 6(4) :RWR-0029-2018. http://dx.doi.org/10.1128/microbiolspec.RWR-0029-2018. [PubMed]
38. Akopian D, Shen K, Zhang X, Shan SO. 2013. Signal recognition particle: an essential protein-targeting machine. Annu Rev Biochem 82:693–721 http://dx.doi.org/10.1146/annurev-biochem-072711-164732. [PubMed]
39. Mondragón A. 2013. Structural studies of RNase P. Annu Rev Biophys 42:537–557 http://dx.doi.org/10.1146/annurev-biophys-083012-130406. [PubMed]
40. Keiler KC. 2015. Mechanisms of ribosome rescue in bacteria. Nat Rev Microbiol 13:285–297 http://dx.doi.org/10.1038/nrmicro3438. [PubMed]
41. Ranquet C, Gottesman S. 2007. Translational regulation of the Escherichia coli stress factor RpoS: a role for SsrA and Lon. J Bacteriol 189:4872–4879 http://dx.doi.org/10.1128/JB.01838-06. [PubMed]
42. Wassarman KM. 2018. 6S RNA, a global regulator of transcription. Microbiol Spectr 6(3) :RWR-0019-2018. http://dx.doi.org/10.1128/microbiolspec.RWR-0019-2018. [PubMed]
43. Sim S, Wolin SL. 2018. Bacterial Y RNAs: gates, tethers, and tRNA mimics. Microbiol Spectr 6(4) :RWR-0023-2018. http://dx.doi.org/10.1128/microbiolspec.RWR-0023-2018. [PubMed]
44. Masachis S, Darfeuille F. 2018. Type I toxin-antitoxin systems: regulating toxin expression via Shine-Dalgarno sequence sequestration and small RNA binding. Microbiol Spectr 6(4) :RWR-0030-2018. http://dx.doi.org/10.1128/microbiolspec.RWR-0030-2018. [PubMed]
45. Vogel J, Argaman L, Wagner EGH, Altuvia S. 2004. The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol 14:2271–2276 http://dx.doi.org/10.1016/j.cub.2004.12.003. [PubMed]
46. Darfeuille F, Unoson C, Vogel J, Wagner EGH. 2007. An antisense RNA inhibits translation by competing with standby ribosomes. Mol Cell 26:381–392 http://dx.doi.org/10.1016/j.molcel.2007.04.003. [PubMed]
47. Opdyke JA, Kang JG, Storz G. 2004. GadY, a small-RNA regulator of acid response genes in Escherichia coli. J Bacteriol 186:6698–6705 http://dx.doi.org/10.1128/JB.186.20.6698-6705.2004. [PubMed]
48. Opdyke JA, Fozo EM, Hemm MR, Storz G. 2011. RNase III participates in GadY-dependent cleavage of the gadX-gadW mRNA. J Mol Biol 406:29–43 http://dx.doi.org/10.1016/j.jmb.2010.12.009. [PubMed]
49. Aiso T, Kamiya S, Yonezawa H, Gamou S. 2014. Overexpression of an antisense RNA, ArrS, increases the acid resistance of Escherichia coli. Microbiology 160:954–961 http://dx.doi.org/10.1099/mic.0.075994-0. [PubMed]
50. Choi JS, Kim W, Suk S, Park H, Bak G, Yoon J, Lee Y. 2018. The small RNA, SdsR, acts as a novel type of toxin in Escherichia coli. RNA Biol 15:1319–1335 http://dx.doi.org/10.1080/15476286.2018.1532252. [PubMed]
51. Fröhlich KS, Haneke K, Papenfort K, Vogel J. 2016. The target spectrum of SdsR small RNA in Salmonella. Nucleic Acids Res 44:10406–10422. [PubMed]
52. Parker A, Gottesman S. 2016. Small RNA regulation of TolC, the outer membrane component of bacterial multidrug transporters. J Bacteriol 198:1101–1113 http://dx.doi.org/10.1128/JB.00971-15. [PubMed]
53. Fontaine F, Gasiorowski E, Gracia C, Ballouche M, Caillet J, Marchais A, Hajnsdorf E. 2016. The small RNA SraG participates in PNPase homeostasis. RNA 22:1560–1573 http://dx.doi.org/10.1261/rna.055236.115. [PubMed]
54. Babitzke P, Lai YJ, Renda AJ, Romeo T. 2019. Posttranscription initiation control of gene expression mediated by bacterial RNA-binding proteins. Annu Rev Microbiol 73:43–67 http://dx.doi.org/10.1146/annurev-micro-020518-115907. [PubMed]
55. Holmqvist E, Vogel J. 2018. RNA-binding proteins in bacteria. Nat Rev Microbiol 16:601–615 http://dx.doi.org/10.1038/s41579-018-0049-5. [PubMed]
56. Franze de Fernandez MT, Eoyang L, August JT. 1968. Factor fraction required for the synthesis of bacteriophage Qbeta-RNA. Nature 219:588–590 http://dx.doi.org/10.1038/219588a0. [PubMed]
57. Updegrove TB, Zhang A, Storz G. 2016. Hfq: the flexible RNA matchmaker. Curr Opin Microbiol 30:133–138 http://dx.doi.org/10.1016/j.mib.2016.02.003. [PubMed]
58. Woodson SA, Panja S, Santiago-Frangos A. 2018. Proteins that chaperone RNA regulation. Microbiol Spectr 6(4) :RWR-0026-2018. http://dx.doi.org/10.1128/microbiolspec.RWR-0026-2018. [PubMed]
59. Schu DJ, Zhang A, Gottesman S, Storz G. 2015. Alternative Hfq-sRNA interaction modes dictate alternative mRNA recognition. EMBO J 34:2557–2573 http://dx.doi.org/10.15252/embj.201591569. [PubMed]
60. Zhang A, Schu DJ, Tjaden BC, Storz G, Gottesman S. 2013. Mutations in interaction surfaces differentially impact E. coli Hfq association with small RNAs and their mRNA targets. J Mol Biol 425:3678–3697 http://dx.doi.org/10.1016/j.jmb.2013.01.006. [PubMed]
61. Santiago-Frangos A, Kavita K, Schu DJ, Gottesman S, Woodson SA. 2016. C-terminal domain of the RNA chaperone Hfq drives sRNA competition and release of target RNA. Proc Natl Acad Sci USA 113:E6089–E6096 http://dx.doi.org/10.1073/pnas.1613053113. [PubMed]
62. Panja S, Santiago-Frangos A, Schu DJ, Gottesman S, Woodson SA. 2015. Acidic residues in the Hfq chaperone increase the selectivity of sRNA binding and annealing. J Mol Biol 427:3491–3500 http://dx.doi.org/10.1016/j.jmb.2015.07.010. [PubMed]
63. Santiago-Frangos A, Jeliazkov JR, Gray JJ, Woodson SA. 2017. Acidic C-terminal domains autoregulate the RNA chaperone Hfq. eLife 6:e27049 http://dx.doi.org/10.7554/eLife.27049. [PubMed]
64. Wagner EGH. 2013. Cycling of RNAs on Hfq. RNA Biol 10:619–626 http://dx.doi.org/10.4161/rna.24044. [PubMed]
65. Malabirade A, Morgado-Brajones J, Trépout S, Wien F, Marquez I, Seguin J, Marco S, Velez M, Arluison V. 2017. Membrane association of the bacterial riboregulator Hfq and functional perspectives. Sci Rep 7:10724 http://dx.doi.org/10.1038/s41598-017-11157-5. [PubMed]
66. Persson F, Lindén M, Unoson C, Elf J. 2013. Extracting intracellular diffusive states and transition rates from single-molecule tracking data. Nat Methods 10:265–269 http://dx.doi.org/10.1038/nmeth.2367. [PubMed]
67. Kannaiah S, Livny J, Amster-Choder O. 2019. Spatiotemporal organization of the E. coli transcriptome: translation independence and engagement in regulation. Mol Cell 76:574–589.e7 http://dx.doi.org/10.1016/j.molcel.2019.08.013. [PubMed]
68. Olejniczak M, Storz G. 2017. ProQ/FinO-domain proteins: another ubiquitous family of RNA matchmakers? Mol Microbiol 104:905–915 http://dx.doi.org/10.1111/mmi.13679. [PubMed]
69. Stalmach ME, Grothe S, Wood JM. 1983. Two proline porters in Escherichia coli K-12. J Bacteriol 156:481–486 http://dx.doi.org/10.1128/JB.156.2.481-486.1983. [PubMed]
70. Milner JL, Wood JM. 1989. Insertion proQ220:Tn 5 alters regulation of proline porter II, a transporter of proline and glycine betaine in Escherichia coli. J Bacteriol 171:947–951 http://dx.doi.org/10.1128/JB.171.2.947-951.1989. [PubMed]
71. Gonzalez GM, Hardwick SW, Maslen SL, Skehel JM, Holmqvist E, Vogel J, Bateman A, Luisi BF, Broadhurst RW. 2017. Structure of the Escherichia coli ProQ RNA-binding protein. RNA 23:696–711 http://dx.doi.org/10.1261/rna.060343.116. [PubMed]
72. Smirnov A, Wang C, Drewry LL, Vogel J. 2017. Molecular mechanism of mRNA repression in trans by a ProQ-dependent small RNA. EMBO J 36:1029–1045 http://dx.doi.org/10.15252/embj.201696127. [PubMed]
73. Westermann AJ, Venturini E, Sellin ME, Förstner KU, Hardt WD, Vogel J. 2019. The major RNA-binding protein ProQ impacts virulence gene expression in Salmonella enterica serovar Typhimurium. MBio 10:e02504-18 http://dx.doi.org/10.1128/mBio.02504-18. [PubMed]
74. Romeo T, Babitzke P. 2018. Global regulation by CsrA and its RNA antagonists. Microbiol Spectr 6(2) :RWR-0009-2017. http://dx.doi.org/10.1128/microbiolspec.RWR-0009-2017. [PubMed]
75. Gutiérrez P, Li Y, Osborne MJ, Pomerantseva E, Liu Q, Gehring K. 2005. Solution structure of the carbon storage regulator protein CsrA from Escherichia coli. J Bacteriol 187:3496–3501 http://dx.doi.org/10.1128/JB.187.10.3496-3501.2005. [PubMed]
76. Timmermans J, Van Melderen L. 2009. Conditional essentiality of the csrA gene in Escherichia coli. J Bacteriol 191:1722–1724 http://dx.doi.org/10.1128/JB.01573-08. [PubMed]
77. Jørgensen MG, Thomason MK, Havelund J, Valentin-Hansen P, Storz G. 2013. Dual function of the McaS small RNA in controlling biofilm formation. Genes Dev 27:1132–1145 http://dx.doi.org/10.1101/gad.214734.113. [PubMed]
78. Sterzenbach T, Nguyen KT, Nuccio SP, Winter MG, Vakulskas CA, Clegg S, Romeo T, Bäumler AJ. 2013. A novel CsrA titration mechanism regulates fimbrial gene expression in Salmonella typhimurium. EMBO J 32:2872–2883 http://dx.doi.org/10.1038/emboj.2013.206. [PubMed]
79. Waters SA, McAteer SP, Kudla G, Pang I, Deshpande NP, Amos TG, Leong KW, Wilkins MR, Strugnell R, Gally DL, Tollervey D, Tree JJ. 2017. Small RNA interactome of pathogenic E. coli revealed through crosslinking of RNase E. EMBO J 36:374–387 http://dx.doi.org/10.15252/embj.201694639. [PubMed]
80. Chao Y, Li L, Girodat D, Förstner KU, Said N, Corcoran C, Śmiga M, Papenfort K, Reinhardt R, Wieden HJ, Luisi BF, Vogel J. 2017. In vivo cleavage map illuminates the central role of RNase E in coding and non-coding RNA pathways. Mol Cell 65:39–51 http://dx.doi.org/10.1016/j.molcel.2016.11.002. [PubMed]
81. Altuvia Y, Bar A, Reiss N, Karavani E, Argaman L, Margalit H. 2018. In vivo cleavage rules and target repertoire of RNase III in Escherichia coli. Nucleic Acids Res 46:10530–10531 http://dx.doi.org/10.1093/nar/gky816. [PubMed]
82. Gordon GC, Cameron JC, Pfleger BF. 2017. RNA sequencing identifies new RNase III cleavage sites in Escherichia coli and reveals increased regulation of mRNA. MBio 8:e00128-17 http://dx.doi.org/10.1128/mBio.00128-17. [PubMed]
83. De Lay N, Gottesman S. 2011. Role of polynucleotide phosphorylase in sRNA function in Escherichia coli. RNA 17:1172–1189 http://dx.doi.org/10.1261/rna.2531211. [PubMed]
84. Cameron TA, Matz LM, Sinha D, De Lay NR. 2019. Polynucleotide phosphorylase promotes the stability and function of Hfq-binding sRNAs by degrading target mRNA-derived fragments. Nucleic Acids Res 47:8821–8837 http://dx.doi.org/10.1093/nar/gkz616. [PubMed]
85. Göpel Y, Papenfort K, Reichenbach B, Vogel J, Görke B. 2013. Targeted decay of a regulatory small RNA by an adaptor protein for RNase E and counteraction by an anti-adaptor RNA. Genes Dev 27:552–564 http://dx.doi.org/10.1101/gad.210112.112. [PubMed]
86. Suzuki K, Babitzke P, Kushner SR, Romeo T. 2006. Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev 20:2605–2617 http://dx.doi.org/10.1101/gad.1461606. [PubMed]
87. Michaux C, Holmqvist E, Vasicek E, Sharan M, Barquist L, Westermann AJ, Gunn JS, Vogel J. 2017. RNA target profiles direct the discovery of virulence functions for the cold-shock proteins CspC and CspE. Proc Natl Acad Sci USA 114:6824–6829 http://dx.doi.org/10.1073/pnas.1620772114. [PubMed]
88. Zhang Y, Burkhardt DH, Rouskin S, Li GW, Weissman JS, Gross CA. 2018. A stress response that monitors and regulates mRNA structure is central to cold shock adaptation. Mol Cell 70:274–286.e7 http://dx.doi.org/10.1016/j.molcel.2018.02.035. [PubMed]
89. Miyakoshi M, Chao Y, Vogel J. 2015. Regulatory small RNAs from the 3′ regions of bacterial mRNAs. Curr Opin Microbiol 24:132–139 http://dx.doi.org/10.1016/j.mib.2015.01.013. [PubMed]
90. Dar D, Sorek R. 2018. Bacterial noncoding RNAs excised from within protein-coding transcripts. MBio 9:e01730-18 http://dx.doi.org/10.1128/mBio.01730-18. [PubMed]
91. Massé E, Escorcia FE, Gottesman S. 2003. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 17:2374–2383 http://dx.doi.org/10.1101/gad.1127103. [PubMed]
92. Morita T, Nishino R, Aiba H. 2017. Role of the terminator hairpin in the biogenesis of functional Hfq-binding sRNAs. RNA 23:1419–1431 http://dx.doi.org/10.1261/rna.060756.117. [PubMed]
93. Massé 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 http://dx.doi.org/10.1073/pnas.032066599.
94. Altuvia S, Weinstein-Fischer D, Zhang A, Postow L, Storz G. 1997. A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 90:43–53 http://dx.doi.org/10.1016/S0092-8674(00)80312-8.
95. Guo MS, Updegrove TB, Gogol EB, Shabalina SA, Gross CA, Storz G. 2014. MicL, a new σE-dependent sRNA, combats envelope stress by repressing synthesis of Lpp, the major outer membrane lipoprotein. Genes Dev 28:1620–1634 http://dx.doi.org/10.1101/gad.243485.114. [PubMed]
96. Morita T, Ueda M, Kubo K, Aiba H. 2015. Insights into transcription termination of Hfq-binding sRNAs of Escherichia coli and characterization of readthrough products. RNA 21:1490–1501 http://dx.doi.org/10.1261/rna.051870.115. [PubMed]
97. Miyakoshi M, Chao Y, Vogel J. 2015. Cross talk between ABC transporter mRNAs via a target mRNA-derived sponge of the GcvB small RNA. EMBO J 34:1478–1492 http://dx.doi.org/10.15252/embj.201490546. [PubMed]
98. Höfer K, Jäschke A. 2018. Epitranscriptomics: RNA modifications in bacteria and archaea. Microbiol Spectr 6(3) :RWR-0015-2017. http://dx.doi.org/10.1128/microbiolspec.RWR-0015-2017. [PubMed]
99. Marbaniang CN, Vogel J. 2016. Emerging roles of RNA modifications in bacteria. Curr Opin Microbiol 30:50–57 http://dx.doi.org/10.1016/j.mib.2016.01.001. [PubMed]
100. Cahová H, Winz ML, Höfer K, Nübel G, Jäschke A. 2015. NAD captureSeq indicates NAD as a bacterial cap for a subset of regulatory RNAs. Nature 519:374–377 http://dx.doi.org/10.1038/nature14020. [PubMed]
101. Deng X, Chen K, Luo GZ, Weng X, Ji Q, Zhou T, He C. 2015. Widespread occurrence of N6-methyladenosine in bacterial mRNA. Nucleic Acids Res 43:6557–6567 http://dx.doi.org/10.1093/nar/gkv596. [PubMed]
102. Bird JG, Zhang Y, Tian Y, Panova N, Barvík I, Greene L, Liu M, Buckley B, Krásný L, Lee JK, Kaplan CD, Ebright RH, Nickels BE. 2016. The mechanism of RNA 5′ capping with NAD+, NADH and desphospho-CoA. Nature 535:444–447 http://dx.doi.org/10.1038/nature18622. [PubMed]
103. De Mets F, Van Melderen L, Gottesman S. 2019. Regulation of acetate metabolism and coordination with the TCA cycle via a processed small RNA. Proc Natl Acad Sci USA 116:1043–1052 http://dx.doi.org/10.1073/pnas.1815288116. [PubMed]
104. Miyakoshi M, Matera G, Maki K, Sone Y, Vogel J. 2019. Functional expansion of a TCA cycle operon mRNA by a 3′ end-derived small RNA. Nucleic Acids Res 47:2075–2088 http://dx.doi.org/10.1093/nar/gky1243. [PubMed]
105. Soper T, Mandin P, Majdalani N, Gottesman S, Woodson SA. 2010. Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci USA 107:9602–9607 http://dx.doi.org/10.1073/pnas.1004435107.
106. Hao Y, Updegrove TB, Livingston NN, Storz G. 2016. Protection against deleterious nitrogen compounds: role of σ S-dependent small RNAs encoded adjacent to sdiA. Nucleic Acids Res 44:6935–6948 http://dx.doi.org/10.1093/nar/gkw404. [PubMed]
107. Viegas SC, Silva IJ, Saramago M, Domingues S, Arraiano CM. 2011. Regulation of the small regulatory RNA MicA by ribonuclease III: a target-dependent pathway. Nucleic Acids Res 39:2918–2930 http://dx.doi.org/10.1093/nar/gkq1239. [PubMed]
108. Lybecker M, Zimmermann B, Bilusic I, Tukhtubaeva N, Schroeder R. 2014. The double-stranded transcriptome of Escherichia coli. Proc Natl Acad Sci USA 111:3134–3139 http://dx.doi.org/10.1073/pnas.1315974111. [PubMed]
109. Figueroa-Bossi N, Bossi L. 2018. Sponges and predators in the small RNA world. Microbiol Spectr 6(4) :RWR-0021-2018. http://dx.doi.org/10.1128/microbiolspec.RWR-0021-2018. [PubMed]
110. Figueroa-Bossi N, Valentini M, Malleret L, Fiorini F, Bossi L. 2009. Caught at its own game: regulatory small RNA inactivated by an inducible transcript mimicking its target. Genes Dev 23:2004–2015 http://dx.doi.org/10.1101/gad.541609. [PubMed]
111. Overgaard M, Johansen J, Møller-Jensen J, Valentin-Hansen P. 2009. Switching off small RNA regulation with trap-mRNA. Mol Microbiol 73:790–800 http://dx.doi.org/10.1111/j.1365-2958.2009.06807.x. [PubMed]
112. Göpel Y, Khan MA, Görke B. 2014. Ménage à trois: post-transcriptional control of the key enzyme for cell envelope synthesis by a base-pairing small RNA, an RNase adaptor protein, and a small RNA mimic. RNA Biol 11:433–442 http://dx.doi.org/10.4161/rna.28301.
113. Lalaouna D, Carrier MC, Semsey S, Brouard JS, Wang J, Wade JT, Massé E. 2015. A 3′ external transcribed spacer in a tRNA transcript acts as a sponge for small RNAs to prevent transcriptional noise. Mol Cell 58:393–405 http://dx.doi.org/10.1016/j.molcel.2015.03.013. [PubMed]
114. Sinha D, Matz LM, Cameron TA, De Lay NR. 2018. Poly(A) polymerase is required for RyhB sRNA stability and function in Escherichia coli. RNA 24:1496–1511 http://dx.doi.org/10.1261/rna.067181.118. [PubMed]
115. Raina M, King A, Bianco C, Vanderpool CK. 2018. Dual-function RNAs. Microbiol Spectr 6(5) :RWR-0032-2018. http://dx.doi.org/10.1128/microbiolspec.RWR-0032-2018. [PubMed]
116. Papenfort K, Vanderpool CK. 2015. Target activation by regulatory RNAs in bacteria. FEMS Microbiol Rev 39:362–378 http://dx.doi.org/10.1093/femsre/fuv016. [PubMed]
117. Sharma CM, Darfeuille F, Plantinga TH, Vogel J. 2007. A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. Genes Dev 21:2804–2817 http://dx.doi.org/10.1101/gad.447207. [PubMed]
118. Vanderpool CK, Gottesman S. 2004. Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol 54:1076–1089 http://dx.doi.org/10.1111/j.1365-2958.2004.04348.x. [PubMed]
119. Papenfort K, Bouvier M, Mika F, Sharma CM, Vogel J. 2010. Evidence for an autonomous 5′ target recognition domain in an Hfq-associated small RNA. Proc Natl Acad Sci USA 107:20435–20440 http://dx.doi.org/10.1073/pnas.1009784107. [PubMed]
120. Wright PR, Richter AS, Papenfort K, Mann M, Vogel J, Hess WR, Backofen R, Georg J. 2013. Comparative genomics boosts target prediction for bacterial small RNAs. Proc Natl Acad Sci USA 110:E3487–E3496 http://dx.doi.org/10.1073/pnas.1303248110. [PubMed]
121. Rice JB, Balasubramanian D, Vanderpool CK. 2012. Small RNA binding-site multiplicity involved in translational regulation of a polycistronic mRNA. Proc Natl Acad Sci USA 109:E2691–E2698 http://dx.doi.org/10.1073/pnas.1207927109. [PubMed]
122. Corcoran CP, Podkaminski D, Papenfort K, Urban JH, Hinton JC, Vogel J. 2012. Superfolder GFP reporters validate diverse new mRNA targets of the classic porin regulator, MicF RNA. Mol Microbiol 84:428–445 http://dx.doi.org/10.1111/j.1365-2958.2012.08031.x. [PubMed]
123. 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 http://dx.doi.org/10.1016/j.molcel.2015.12.023. [PubMed]
124. Bouvier M, Sharma CM, Mika F, Nierhaus KH, Vogel J. 2008. Small RNA binding to 5′ mRNA coding region inhibits translational initiation. Mol Cell 32:827–837 http://dx.doi.org/10.1016/j.molcel.2008.10.027. [PubMed]
125. Jagodnik J, Chiaruttini C, Guillier M. 2017. Stem-loop structures within mRNA coding sequences activate translation initiation and mediate control by small regulatory RNAs. Mol Cell 68:158–170.e3 http://dx.doi.org/10.1016/j.molcel.2017.08.015. [PubMed]
126. Azam MS, Vanderpool CK. 2018. Translational regulation by bacterial small RNAs via an unusual Hfq-dependent mechanism. Nucleic Acids Res 46:2585–2599 http://dx.doi.org/10.1093/nar/gkx1286. [PubMed]
127. Hoekzema M, Romilly C, Holmqvist E, Wagner EGH. 2019. Hfq-dependent mRNA unfolding promotes sRNA-based inhibition of translation. EMBO J 38:e101199 http://dx.doi.org/10.15252/embj.2018101199. [PubMed]
128. Chen J, Gottesman S. 2017. Hfq links translation repression to stress-induced mutagenesis in E. coli. Genes Dev 31:1382–1395 http://dx.doi.org/10.1101/gad.302547.117. [PubMed]
129. Majdalani N, Cunning C, Sledjeski D, Elliott T, Gottesman S. 1998. DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc Natl Acad Sci USA 95:12462–12467 http://dx.doi.org/10.1073/pnas.95.21.12462. [PubMed]
130. Prévost K, Salvail H, Desnoyers G, Jacques JF, Phaneuf E, Massé 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 http://dx.doi.org/10.1111/j.1365-2958.2007.05733.x. [PubMed]
131. Urban JH, Vogel J. 2008. Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol 6:e64 http://dx.doi.org/10.1371/journal.pbio.0060064. [PubMed]
132. Salvail H, Caron MP, Bélanger J, Massé E. 2013. Antagonistic functions between the RNA chaperone Hfq and an sRNA regulate sensitivity to the antibiotic colicin. EMBO J 32:2764–2778 http://dx.doi.org/10.1038/emboj.2013.205. [PubMed]
133. Pfeiffer V, Papenfort K, Lucchini S, Hinton JC, Vogel J. 2009. Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat Struct Mol Biol 16:840–846 http://dx.doi.org/10.1038/nsmb.1631. [PubMed]
134. Bandyra KJ, Said N, Pfeiffer V, Górna MW, Vogel J, Luisi BF. 2012. The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol Cell 47:943–953 http://dx.doi.org/10.1016/j.molcel.2012.07.015. [PubMed]
135. Göpel Y, Khan MA, Görke B. 2016. Domain swapping between homologous bacterial small RNAs dissects processing and Hfq binding determinants and uncovers an aptamer for conditional RNase E cleavage. Nucleic Acids Res 44:824–837 http://dx.doi.org/10.1093/nar/gkv1161. [PubMed]
136. Andreassen PR, Pettersen JS, Szczerba M, Valentin-Hansen P, Møller-Jensen J, Jørgensen MG. 2018. sRNA-dependent control of curli biosynthesis in Escherichia coli: McaS directs endonucleolytic cleavage of csgD mRNA. Nucleic Acids Res 46:6746–6760 http://dx.doi.org/10.1093/nar/gky479. [PubMed]
137. Papenfort K, Sun Y, Miyakoshi M, Vanderpool CK, Vogel J. 2013. Small RNA-mediated activation of sugar phosphatase mRNA regulates glucose homeostasis. Cell 153:426–437 http://dx.doi.org/10.1016/j.cell.2013.03.003. [PubMed]
138. Fröhlich KS, Papenfort K, Fekete A, Vogel J. 2013. A small RNA activates CFA synthase by isoform-specific mRNA stabilization. EMBO J 32:2963–2979 http://dx.doi.org/10.1038/emboj.2013.222. [PubMed]
139. Chen J, Morita T, Gottesman S. 2019. Regulation of transcription termination of small RNAs and by small RNAs: molecular mechanisms and biological functions. Front Cell Infect Microbiol 9:201 http://dx.doi.org/10.3389/fcimb.2019.00201. [PubMed]
140. Bossi L, Schwartz A, Guillemardet B, Boudvillain M, Figueroa-Bossi N. 2012. A role for Rho-dependent polarity in gene regulation by a noncoding small RNA. Genes Dev 26:1864–1873 http://dx.doi.org/10.1101/gad.195412.112. [PubMed]
141. Sedlyarova N, Shamovsky I, Bharati BK, Epshtein V, Chen J, Gottesman S, Schroeder R, Nudler E. 2016. sRNA-mediated control of transcription termination in E. coli. Cell 167:111–121.e13 http://dx.doi.org/10.1016/j.cell.2016.09.004. [PubMed]
142. Silva IJ, Barahona S, Eyraud A, Lalaouna D, Figueroa-Bossi N, Massé E, Arraiano CM. 2019. SraL sRNA interaction regulates the terminator by preventing premature transcription termination of rho mRNA. Proc Natl Acad Sci USA 116:3042–3051 http://dx.doi.org/10.1073/pnas.1811589116. [PubMed]
143. Brosse A, Guillier M. 2018. Bacterial small RNAs in mixed regulatory networks. Microbiol Spectr 6(3) :RWR-0014-2017. http://dx.doi.org/10.1128/microbiolspec.RWR-0014-2017. [PubMed]
144. Nitzan M, Rehani R, Margalit H. 2017. Integration of bacterial small RNAs in regulatory networks. Annu Rev Biophys 46:131–148 http://dx.doi.org/10.1146/annurev-biophys-070816-034058. [PubMed]
145. Brosse A, Korobeinikova A, Gottesman S, Guillier M. 2016. Unexpected properties of sRNA promoters allow feedback control via regulation of a two-component system. Nucleic Acids Res 44:9650–9666 http://dx.doi.org/10.1093/nar/gkw642. [PubMed]
146. Guillier M, Gottesman S. 2008. The 5′ end of two redundant sRNAs is involved in the regulation of multiple targets, including their own regulator. Nucleic Acids Res 36:6781–6794 http://dx.doi.org/10.1093/nar/gkn742. [PubMed]
147. Gogol EB, Rhodius VA, Papenfort K, Vogel J, Gross CA. 2011. Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon. Proc Natl Acad Sci USA 108:12875–12880 http://dx.doi.org/10.1073/pnas.1109379108.
148. Hör J, Gorski SA, Vogel J. 2018. Bacterial RNA biology on a genome scale. Mol Cell 70:785–799 http://dx.doi.org/10.1016/j.molcel.2017.12.023. [PubMed]
149. Lopez CA, Skaar EP. 2018. The impact of dietary transition metals on host-bacterial interactions. Cell Host Microbe 23:737–748 http://dx.doi.org/10.1016/j.chom.2018.05.008. [PubMed]
150. Chareyre S, Mandin P. 2018. Bacterial iron homeostasis regulation by sRNAs. Microbiol Spectr 6(2) :RWR-0010-2017. http://dx.doi.org/10.1128/microbiolspec.RWR-0010-2017. [PubMed]
151. Salvail H, Lanthier-Bourbonnais P, Sobota JM, Caza M, Benjamin JA, Mendieta ME, Lépine F, Dozois CM, Imlay J, Massé E. 2010. A small RNA promotes siderophore production through transcriptional and metabolic remodeling. Proc Natl Acad Sci USA 107:15223–15228 http://dx.doi.org/10.1073/pnas.1007805107. [PubMed]
152. Jacques JF, Jang S, Prévost K, Desnoyers G, Desmarais M, Imlay J, Massé E. 2006. RyhB small RNA modulates the free intracellular iron pool and is essential for normal growth during iron limitation in Escherichia coli. Mol Microbiol 62:1181–1190 http://dx.doi.org/10.1111/j.1365-2958.2006.05439.x. [PubMed]
153. Kim JN. 2016. Roles of two RyhB paralogs in the physiology of Salmonella enterica. Microbiol Res 186-187:146–152 http://dx.doi.org/10.1016/j.micres.2016.04.004. [PubMed]
154. Ikemura T, Dahlberg JE. 1973. Small ribonucleic acids of Escherichia coli. II. Noncoordinate accumulation during stringent control. J Biol Chem 248:5033–5041.
155. Sahagan BG, Dahlberg JE. 1979. A small, unstable RNA molecule of Escherichia coli: Spot 42 RNA. II. Accumulation and distribution. J Mol Biol 131:593–605 http://dx.doi.org/10.1016/0022-2836(79)90009-3.
156. Polayes DA, Rice PW, Garner MM, Dahlberg JE. 1988. Cyclic AMP-cyclic AMP receptor protein as a repressor of transcription of the spf gene of Escherichia coli. J Bacteriol 170:3110–3114 http://dx.doi.org/10.1128/JB.170.7.3110-3114.1988. [PubMed]
157. Møller T, Franch T, Udesen C, Gerdes K, Valentin-Hansen P. 2002. Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev 16:1696–1706 http://dx.doi.org/10.1101/gad.231702. [PubMed]
158. Møller T, Franch T, Højrup P, Keene DR, Bächinger HP, Brennan RG, Valentin-Hansen P. 2002. Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol Cell 9:23–30 http://dx.doi.org/10.1016/S1097-2765(01)00436-1.
159. Lewis DE, Adhya S. 2015. Molecular mechanisms of transcription initiation at gal promoters and their multi-level regulation by GalR, CRP and DNA loop. Biomolecules 5:2782–2807 http://dx.doi.org/10.3390/biom5042782. [PubMed]
160. Beisel CL, Storz G. 2011. The base-pairing RNA Spot 42 participates in a multioutput feedforward loop to help enact catabolite repression in Escherichia coli. Mol Cell 41:286–297 http://dx.doi.org/10.1016/j.molcel.2010.12.027. [PubMed]
161. Durica-Mitic S, Göpel Y, Görke B. 2018. Carbohydrate utilization in bacteria: making the most out of sugars with the help of small regulatory RNAs. Microbiol Spectr 6(2) :RWR-0013-2017. 10.1128/microbiolspec.RWR-0013-2017. [PubMed]
162. Thomason MK, Fontaine F, De Lay N, Storz G. 2012. A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. Mol Microbiol 84:17–35 http://dx.doi.org/10.1111/j.1365-2958.2012.07965.x. [PubMed]
163. Papenfort K, Pfeiffer V, Lucchini S, Sonawane A, Hinton JC, Vogel J. 2008. Systematic deletion of Salmonella small RNA genes identifies CyaR, a conserved CRP-dependent riboregulator of OmpX synthesis. Mol Microbiol 68:890–906 http://dx.doi.org/10.1111/j.1365-2958.2008.06189.x. [PubMed]
164. De Lay N, Gottesman S. 2009. The Crp-activated sRNA CyaR (RyeE) links nutritional status to group behavior. J Bacteriol 191:461–476 http://dx.doi.org/10.1128/JB.01157-08. [PubMed]
165. Guisbert E, Rhodius VA, Ahuja N, Witkin E, Gross CA. 2007. Hfq modulates the sigmaE-mediated envelope stress response and the sigma32-mediated cytoplasmic stress response in Escherichia coli. J Bacteriol 189:1963–1973 http://dx.doi.org/10.1128/JB.01243-06. [PubMed]
166. Lonetto MA, Donohue TJ, Gross CA, Buttner MJ. 2019. Discovery of the extracytoplasmic function σ factors. Mol Microbiol 112:348–355 http://dx.doi.org/10.1111/mmi.14307. [PubMed]
167. Johansen J, Rasmussen AA, Overgaard M, Valentin-Hansen P. 2006. Conserved small non-coding RNAs that belong to the sigmaE regulon: role in down-regulation of outer membrane proteins. J Mol Biol 364:1–8 http://dx.doi.org/10.1016/j.jmb.2006.09.004. [PubMed]
168. Thompson KM, Rhodius VA, Gottesman S. 2007. SigmaE regulates and is regulated by a small RNA in Escherichia coli. J Bacteriol 189:4243–4256 http://dx.doi.org/10.1128/JB.00020-07. [PubMed]
169. Papenfort K, Pfeiffer V, Mika F, Lucchini S, Hinton JC, Vogel J. 2006. SigmaE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 62:1674–1688 http://dx.doi.org/10.1111/j.1365-2958.2006.05524.x. [PubMed]
170. Grabowicz M, Koren D, Silhavy TJ. 2016. The CpxQ sRNA negatively regulates Skp to prevent mistargeting of β-barrel outer membrane proteins into the cytoplasmic membrane. MBio 7:e00312-16 http://dx.doi.org/10.1128/mBio.00312-16. [PubMed]
171. Gottesman S. 2019. Trouble is coming: signaling pathways that regulate general stress responses in bacteria. J Biol Chem 294:11685–11700 http://dx.doi.org/10.1074/jbc.REV119.005593. [PubMed]
172. Majdalani N, Hernandez D, Gottesman S. 2002. Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46:813–826 http://dx.doi.org/10.1046/j.1365-2958.2002.03203.x. [PubMed]
173. Mandin P, Gottesman S. 2010. Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 29:3094–3107 http://dx.doi.org/10.1038/emboj.2010.179. [PubMed]
174. Sledjeski DD, Gupta A, Gottesman S. 1996. The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J 15:3993–4000 http://dx.doi.org/10.1002/j.1460-2075.1996.tb00773.x. [PubMed]
175. Repoila F, Gottesman S. 2003. Temperature sensing by the dsrA promoter. J Bacteriol 185:6609–6614 http://dx.doi.org/10.1128/JB.185.22.6609-6614.2003. [PubMed]
176. Girard ME, Gopalkrishnan S, Grace ED, Halliday JA, Gourse RL, Herman C. 2017. DksA and ppGpp regulate the σS stress response by activating promoters for the small RNA DsrA and the anti-adapter protein IraP. J Bacteriol 200:e00463-17 http://dx.doi.org/10.1128/JB.00463-17. [PubMed]
177. Wall E, Majdalani N, Gottesman S. 2018. The complex Rcs regulatory cascade. Annu Rev Microbiol 72:111–139 http://dx.doi.org/10.1146/annurev-micro-090817-062640. [PubMed]
178. Papenfort K, Said N, Welsink T, Lucchini S, Hinton JCD, Vogel J. 2009. Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 74:139–158 http://dx.doi.org/10.1111/j.1365-2958.2009.06857.x. [PubMed]
179. Mika F, Hengge R. 2014. Small RNAs in the control of RpoS, CsgD, and biofilm architecture of Escherichia coli. RNA Biol 11:494–507 http://dx.doi.org/10.4161/rna.28867. [PubMed]
180. Mika F, Busse S, Possling A, Berkholz J, Tschowri N, Sommerfeldt N, Pruteanu M, Hengge R. 2012. Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Mol Microbiol 84:51–65 http://dx.doi.org/10.1111/j.1365-2958.2012.08002.x. [PubMed]
181. De Lay N, Gottesman S. 2012. A complex network of small non-coding RNAs regulate motility in Escherichia coli. Mol Microbiol 86:524–538 http://dx.doi.org/10.1111/j.1365-2958.2012.08209.x. [PubMed]
182. Fröhlich KS, Papenfort K, Berger AA, Vogel J. 2012. A conserved RpoS-dependent small RNA controls the synthesis of major porin OmpD. Nucleic Acids Res 40:3623–3640 http://dx.doi.org/10.1093/nar/gkr1156. [PubMed]
183. Chao Y, Vogel J. 2010. The role of Hfq in bacterial pathogens. Curr Opin Microbiol 13:24–33 http://dx.doi.org/10.1016/j.mib.2010.01.001. [PubMed]
184. Westermann AJ. 2018. Regulatory RNAs in virulence and host-microbe interactions. Microbiol Spectr 6(4) :RWR-0002-2017. http://dx.doi.org/10.1128/microbiolspec.RWR-0002-2017. [PubMed]
185. Westermann AJ, Förstner KU, Amman F, Barquist L, Chao Y, Schulte LN, Müller L, Reinhardt R, Stadler PF, Vogel J. 2016. Dual RNA-seq unveils noncoding RNA functions in host-pathogen interactions. Nature 529:496–501 http://dx.doi.org/10.1038/nature16547. [PubMed]
186. Kim K, Palmer AD, Vanderpool CK, Slauch JM. 2019. The small RNA PinT contributes to PhoP-mediated regulation of the Salmonella pathogenicity island 1 type III secretion system in Salmonella enterica serovar Typhimurium. J Bacteriol 201:e00312-19 http://dx.doi.org/10.1128/JB.00312-19. [PubMed]
187. El Mouali Y, Gaviria-Cantin T, Sánchez-Romero MA, Gibert M, Westermann AJ, Vogel J, Balsalobre C. 2018. CRP-cAMP mediates silencing of Salmonella virulence at the post-transcriptional level. PLoS Genet 14:e1007401 http://dx.doi.org/10.1371/journal.pgen.1007401. [PubMed]
188. Song M, Sukovich DJ, Ciccarelli L, Mayr J, Fernandez-Rodriguez J, Mirsky EA, Tucker AC, Gordon DB, Marlovits TC, Voigt CA. 2017. Control of type III protein secretion using a minimal genetic system. Nat Commun 8:14737 http://dx.doi.org/10.1038/ncomms14737. [PubMed]
189. Papenfort K, Podkaminski D, Hinton JC, Vogel J. 2012. The ancestral SgrS RNA discriminates horizontally acquired Salmonella mRNAs through a single G-U wobble pair. Proc Natl Acad Sci USA 109:E757–E764 http://dx.doi.org/10.1073/pnas.1119414109. [PubMed]
190. Barquist L, Westermann AJ, Vogel J. 2016. Molecular phenotyping of infection-associated small non-coding RNAs. Philos Trans R Soc Lond B Biol Sci 371:20160081 http://dx.doi.org/10.1098/rstb.2016.0081. [PubMed]
Loading

Article metrics loading...

/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0030-2019
2020-03-20
2020-11-24

Abstract:

The last few decades have led to an explosion in our understanding of the major roles that small regulatory RNAs (sRNAs) play in regulatory circuits and the responses to stress in many bacterial species. Much of the foundational work was carried out with and serovar Typhimurium. The studies of these organisms provided an overview of how the sRNAs function and their impact on bacterial physiology, serving as a blueprint for sRNA biology in many other prokaryotes. They also led to the development of new technologies. In this chapter, we first summarize how these sRNAs were identified, defining them in the process. We discuss how they are regulated and how they act and provide selected examples of their roles in regulatory circuits and the consequences of this regulation. Throughout, we summarize the methodologies that were developed to identify and study the regulatory RNAs, most of which are applicable to other bacteria. Newly updated databases of the known sRNAs in K-12 and Typhimurium SL1344 serve as a reference point for much of the discussion and, hopefully, as a resource for readers and for future experiments to address open questions raised in this review.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/ecosalplus/9/1/ESP-0030-2019.html?itemId=/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0030-2019&mimeType=html&fmt=ahah
Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed

Figures

Trans-Acting Small RNAs and Their Effects on Gene Expression in and
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-1,webId=/content/author/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-1,properties={foaf_givenname=Jens, foaf_name=Jens Hör, foaf_surname=Hör, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-2,webId=/content/author/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-2,properties={foaf_givenname=Gianluca, foaf_name=Gianluca Matera, foaf_surname=Matera, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-3,webId=/content/author/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-3,properties={foaf_givenname=Jörg, foaf_name=Jörg Vogel, foaf_surname=Vogel, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-aff3],com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-aff4]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-4,webId=/content/author/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-4,properties={foaf_givenname=Susan, foaf_name=Susan Gottesman, foaf_surname=Gottesman, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-aff5]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-5,webId=/content/author/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-5,properties={foaf_givenname=Gisela, foaf_name=Gisela Storz, foaf_surname=Storz, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0030-2019-aff6]]}]]
Citation: Hör J, Matera G, Vogel J, Gottesman S, Storz G. 2020. Trans-Acting Small RNAs and Their Effects on Gene Expression in and , EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0030-2019
/content/ecosalplus/10.1128/ecosalplus.ESP-0030-2019.fig1
Figure 1
Overview of sRNA sources, mechanisms by which their levels and activities are regulated, and mechanisms of action.
ecosalplus/9/1/ESP-0030-2019_fig_001_thmb.gif
ecosalplus/9/1/ESP-0030-2019_fig_001.gif
Image of Figure 1

Click to view

Figure 1

Overview of sRNA sources, mechanisms by which their levels and activities are regulated, and mechanisms of action.

Citation: Hör J, Matera G, Vogel J, Gottesman S, Storz G. 2020. Trans-Acting Small RNAs and Their Effects on Gene Expression in and , EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0030-2019
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/ecosalplus/10.1128/ecosalplus.ESP-0030-2019.fig2
Figure 2
Results of some of the approaches (in italics) are shown for the MicL sRNA ( 95 ).
ecosalplus/9/1/ESP-0030-2019_fig_002_thmb.gif
ecosalplus/9/1/ESP-0030-2019_fig_002.gif
Image of Figure 2

Click to view

Figure 2

Results of some of the approaches (in italics) are shown for the MicL sRNA ( 95 ).

Citation: Hör J, Matera G, Vogel J, Gottesman S, Storz G. 2020. Trans-Acting Small RNAs and Their Effects on Gene Expression in and , EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0030-2019
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/ecosalplus/10.1128/ecosalplus.ESP-0030-2019.fig3
Figure 3
(A) Response to low iron regulated by RyhB. (B) Bias toward glucose utilization regulated by Spot 42. (C) Outer membrane protein (OMP) synthesis controlled by RybB, MicA, and MicL and inner membrane protein (IMP) synthesis controlled by CpxQ. (D) Regulation of the general stress response by multiple sRNAs. (E) Regulation of the transition between virulence programs in by PinT.
ecosalplus/9/1/ESP-0030-2019_fig_003_thmb.gif
ecosalplus/9/1/ESP-0030-2019_fig_003.gif
Image of Figure 3

Click to view

Figure 3

(A) Response to low iron regulated by RyhB. (B) Bias toward glucose utilization regulated by Spot 42. (C) Outer membrane protein (OMP) synthesis controlled by RybB, MicA, and MicL and inner membrane protein (IMP) synthesis controlled by CpxQ. (D) Regulation of the general stress response by multiple sRNAs. (E) Regulation of the transition between virulence programs in by PinT.

Citation: Hör J, Matera G, Vogel J, Gottesman S, Storz G. 2020. Trans-Acting Small RNAs and Their Effects on Gene Expression in and , EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0030-2019
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error