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Small RNAs Regulate Primary and Secondary Metabolism in Gram-negative Bacteria

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  • Authors: Maksym Bobrovskyy1, Carin K. Vanderpool2, Gregory R. Richards3
  • Editors: Tyrrell Conway4, Paul Cohen5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Microbiology, University of Illinois, Urbana, IL 61801; 2: Department of Microbiology, University of Illinois, Urbana, IL 61801; 3: Biological Sciences Department, University of Wisconsin-Parkside, Kenosha, WI 53141; 4: Oklahoma State University, Stillwater, OK; 5: University of Rhode Island, Kingston, RI
  • Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.MBP-0009-2014
  • Received 26 September 2014 Accepted 09 October 2014 Published 18 June 2015
  • Gregory Richards, richarg0@uwp.edu
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  • Abstract:

    Over the last decade, small (often noncoding) RNA molecules have been discovered as important regulators influencing myriad aspects of bacterial physiology and virulence. In particular, small RNAs (sRNAs) have been implicated in control of both primary and secondary metabolic pathways in many bacterial species. This chapter describes characteristics of the major classes of sRNA regulators, and highlights what is known regarding their mechanisms of action. Specific examples of sRNAs that regulate metabolism in gram-negative bacteria are discussed, with a focus on those that regulate gene expression by base pairing with mRNA targets to control their translation and stability.

  • Citation: Bobrovskyy M, Vanderpool C, Richards G. 2015. Small RNAs Regulate Primary and Secondary Metabolism in Gram-negative Bacteria. Microbiol Spectrum 3(3):MBP-0009-2014. doi:10.1128/microbiolspec.MBP-0009-2014.

Key Concept Ranking

Gene Expression and Regulation
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Aromatic Amino Acid Biosynthesis
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Type VI Secretion System
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Bacterial Proteins
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References

1. Masse E, Salvail H, Desnoyers G, Arguin M. 2007. Small RNAs controlling iron metabolism. Cur Opin Microbiol 10:140–145. [PubMed][CrossRef]
2. Vanderpool CK, Gottesman S. 2007. The novel transcription factor SgrR coordinates the response to glucose-phosphate stress. J Bacteriol 189:2238–2248. [PubMed][CrossRef]
3. 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. [PubMed][CrossRef]
4. Frohlich 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. [PubMed][CrossRef]
5. Boysen A, Moller-Jensen J, Kallipolitis B, Valentin-Hansen P, Overgaard M. 2010. Translational regulation of gene expression by an anaerobically induced small non-coding RNA in Escherichia coli. J Biol Chem 285:10690–10702. [PubMed][CrossRef]
6. Storz G, Vogel J, Wassarman KM. 2011. Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43:880–891. [PubMed][CrossRef]
7. Richards GR, Vanderpool CK. 2011. Molecular call and response: the physiology of bacterial small RNAs. Biochim Biophys Acta 1809:525–531. [PubMed][CrossRef]
8. Hoe CH, Raabe CA, Rozhdestvensky TS, Tang TH. 2013. Bacterial sRNAs: regulation in stress. Int J Med Microbiol 303:217–229. [PubMed][CrossRef]
9. Opdyke JA, Kang JG, Storz G. 2004. GadY, a small-RNA regulator of acid response genes in Escherichia coli. J Bacteriol 186:6698–6705. [PubMed][CrossRef]
10. Kawano M, Aravind L, Storz G. 2007. An antisense RNA controls synthesis of an SOS-induced toxin evolved from an antitoxin. Mol Microbiol 64:738–754. [PubMed][CrossRef]
11. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, Balestrino D, Loh E, Gripenland J, Tiensuu T, Vaitkevicius K, Barthelemy M, Vergassola M, Nahori MA, Soubigou G, Regnault B, Coppee JY, Lecuit M, Johansson J, Cossart P. 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950–956. [PubMed][CrossRef]
12. Lee E-J, Groisman E. 2010. An antisense RNA that governs the expression kinetics of a multifunctional virulence gene. Mol Microbiol 76:1020–1033. [PubMed][CrossRef]
13. Stazic D, Lindell D, Steglich C. 2011. Antisense RNA protects mRNA from RNase E degradation by RNA-RNA duplex formation during phage infection. Nucleic Acids Res 39:4890–4899. [PubMed][CrossRef]
14. Wurtzel O, Sesto N, Mellin JR, Karunker I, Edelheit S, Becavin C, Archambaud C, Cossart P, Sorek R. 2012. Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol Sys Biol 8:583. [PubMed][CrossRef]
15. Simons R, Kleckner N. 1983. Translational control of IS10 transposition. Cell 34:683–691. [PubMed][CrossRef]
16. Landt S, Abeliuk E, McGrath P, Lesley J, McAdams H, Shapiro L. 2008. Small non-coding RNAs in Caulobacter crescentus. Mol Microbiol 68:600–614. [PubMed][CrossRef]
17. 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. [PubMed][CrossRef]
18. Waters JL, Salyers AA. 2012. The small RNA RteR inhibits transfer of the Bacteroides conjugative transposon CTnDOT. J Bacteriol 194:5228–5236. [PubMed][CrossRef]
19. Fozo E, Kawano M, Fontaine F, Kaya Y, Mendieta K, Jones K, Ocampo A, Rudd K, Storz G. 2008. Repression of small toxic protein synthesis by the Sib and OhsC small RNAs. Mol Microbiol 70:1076–1093. [PubMed][CrossRef]
20. Fozo E, Makarova K, Shabalina S, Yutin N, Koonin E, Storz G. 2010. Abundance of type I toxin-antitoxin systems in bacteria: searches for new candidates and discovery of novel families. Nucleic Acids Res 38:3743–3759. [PubMed][CrossRef]
21. Georg J, Hess W. 2011. cis-antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75:286–300. [PubMed][CrossRef]
22. Morfeldt E, Taylor D, von Gabain A, Arvidson S. 1995. Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J 14:4569–4577. [PubMed]
23. Lease RA, Cusick ME, Belfort M. 1998. Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. Proc Natl Acad Sci U S A 95:12456–12461. [PubMed][CrossRef]
24. 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. [PubMed][CrossRef]
25. 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. [PubMed]
26. Majdalani N, Chen S, Murrow J, St John K, Gottesman S. 2001. Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol Microbiol 39:1382–1394. [PubMed][CrossRef]
27. Mandin P, Gottesman S. 2010. Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 29:3094–3107. [PubMed][CrossRef]
28. Brown L, Elliott T. 1997. Mutations that increase expression of the rpoS gene and decrease its dependence on hfq function in Salmonella typhimurium. J Bacteriol 179:656–662. [PubMed]
29. Cunning C, Brown L, Elliott T. 1998. Promoter substitution and deletion analysis of upstream region required for rpoS translational regulation. J Bacteriol 180:4564–4570. [PubMed]
30. 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 U S A 95:12462–12467. [PubMed][CrossRef]
31. 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. [PubMed][CrossRef]
32. Mackie G. 1998. Ribonuclease E is a 5′-end-dependent endonuclease. Nature 395:720–723. [PubMed][CrossRef]
33. 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. [PubMed][CrossRef]
34. Frohlich KS, Papenfort K, Fekete A, Vogel J. 2013. A small RNA activates CFA synthase by isoform-specific mRNA stabilization. EMBO J 32:2963–2979. [PubMed][CrossRef]
35. Koonin EV, Tatusov RL. 1994. Computer analysis of bacterial haloacid dehalogenases defines a large superfamily of hydrolases with diverse specificity. Application of an iterative approach to database search. J Mol Biol 244:125–132. [PubMed][CrossRef]
36. Morita T, Mochizuki Y, Aiba H. 2006. Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction. Proc Natl Acad Sci U S A 103:4858–4863. [PubMed][CrossRef]
37. 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. [PubMed][CrossRef]
38. Yang Q, Figueroa-Bossi N, Bossi L. 2014. Translation enhancing ACA motifs and their silencing by a bacterial small regulatory RNA. PLoS Genet 10:e1004026. [PubMed][CrossRef]
39. Darfeuille F, Unoson C, Vogel J, Wagner EG. 2007. An antisense RNA inhibits translation by competing with standby ribosomes. Mol Cell 26:381–392. [PubMed][CrossRef]
40. 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. [PubMed][CrossRef]
41. Beyer D, Skripkin E, Wadzack J, Nierhaus KH. 1994. How the ribosome moves along the mRNA during protein synthesis. J Biol Chem 269:30713–30717. [PubMed]
42. Huttenhofer A, Noller HF. 1994. Footprinting mRNA-ribosome complexes with chemical probes. EMBO J 13:3892–3901. [PubMed]
43. 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. [PubMed][CrossRef]
44. Holmqvist E, Reimegard J, Sterk M, Grantcharova N, Romling U, Wagner EG. 2010. Two antisense RNAs target the transcriptional regulator CsgD to inhibit curli synthesis. EMBO J 29:1840–1850. [PubMed][CrossRef]
45. Desnoyers G, Masse E. 2012. Noncanonical repression of translation initiation through small RNA recruitment of the RNA chaperone Hfq. Genes Devel 26:726–739. [PubMed][CrossRef]
46. Desnoyers G, Bouchard MP, Masse E. 2013. New insights into small RNA-dependent translational regulation in prokaryotes. Trends Genet 29:92–98. [PubMed][CrossRef]
47. Sonnleitner E, Gonzalez N, Sorger-Domenigg T, Heeb S, Richter AS, Backofen R, Williams P, Huttenhofer A, Haas D, Blasi U. 2011. The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal. Mol Microbiol 80:868–885. [PubMed][CrossRef]
48. Masse E, Gottesman S. 2002. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci U S A 99:4620–4625. [PubMed][CrossRef]
49. Masse E, Escorcia FE, Gottesman S. 2003. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Devel 17:2374–2383. [PubMed][CrossRef]
50. Morita T, Maki K, Aiba H. 2005. RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Devel 19:2176–2186. [PubMed][CrossRef]
51. Moller T, Franch T, Udesen C, Gerdes K, Valentin-Hansen P. 2002. Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Devel 16:1696–1706. [PubMed][CrossRef]
52. Pfeiffer V, Papenfort K, Lucchini S, Hinton J, Vogel Jr. 2009. Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat Struct Mol Biol 16:840–846. [PubMed][CrossRef]
53. Carpousis AJ, Luisi BF, McDowall KJ. 2009. Endonucleolytic initiation of mRNA decay in Escherichia coli. Prog Mol Biol Transl Sci 85:91–135. [PubMed][CrossRef]
54. 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. [PubMed][CrossRef]
55. Sneppen K, Dodd I, Shearwin K, Palmer A, Schubert R, Callen B, Egan J. 2005. A mathematical model for transcriptional interference by RNA polymerase traffic in Escherichia coli. J Mol Biol 346:399–409. [PubMed][CrossRef]
56. Crampton N, Bonass W, Kirkham J, Rivetti C, Thomson N. 2006. Collision events between RNA polymerases in convergent transcription studied by atomic force microscopy. Nucleic Acids Res 34:5416–5425. [PubMed][CrossRef]
57. Callen B, Shearwin K, Egan J. 2004. Transcriptional interference between convergent promoters caused by elongation over the promoter. Mol Cell 14:647–656. [PubMed][CrossRef]
58. Palmer A, Ahlgren-Berg A, Egan J, Dodd I, Shearwin K. 2009. Potent transcriptional interference by pausing of RNA polymerases over a downstream promoter. Mol Cell 34:545–555. [PubMed][CrossRef]
59. Andre G, Even S, Putzer H, Burguiere P, Croux C, Danchin A, Martin-Verstraete I, Soutourina O. 2008. S-box and T-box riboswitches and antisense RNA control a sulfur metabolic operon of Clostridium acetobutylicum. Nucleic Acids Res 36:5955–5969. [PubMed][CrossRef]
60. Stork M, Di Lorenzo M, Welch T, Crosa J. 2007. Transcription termination within the iron transport-biosynthesis operon of Vibrio anguillarum requires an antisense RNA. J Bacteriol 189:3479–3488. [PubMed][CrossRef]
61. Giangrossi M, Prosseda G, Tran C, Brandi A, Colonna B, Falconi M. 2010. A novel antisense RNA regulates at transcriptional level the virulence gene icsA of Shigella flexneri. Nucleic Acids Res 38:3362–3375. [PubMed][CrossRef]
62. Wassarman K, Storz G. 2000. 6S RNA regulates E. coli RNA polymerase activity. Cell 101:613–623. [PubMed][CrossRef]
63. Barrick J, Sudarsan N, Weinberg Z, Ruzzo W, Breaker R. 2005. 6S RNA is a widespread regulator of eubacterial RNA polymerase that resembles an open promoter. RNA 11:774–784. [PubMed][CrossRef]
64. Trotochaud A, Wassarman K. 2005. A highly conserved 6S RNA structure is required for regulation of transcription. Nat Struct Mol Biol 12:313–319. [PubMed][CrossRef]
65. Trotochaud A, Wassarman K. 2004. 6S RNA function enhances long-term cell survival. J Bacteriol 186:4978–4985. [PubMed][CrossRef]
66. Cavanagh AT, Klocko AD, Liu X, Wassarman KM. 2008. Promoter specificity for 6S RNA regulation of transcription is determined by core promoter sequences and competition for region 4.2 of sigma70. Mol Microbiol 67:1242–1256. [PubMed][CrossRef]
67. Klocko AD, Wassarman KM. 2009. 6S RNA binding to Esigma(70) requires a positively charged surface of sigma(70) region 4.2. Mol Microbiol 73:152–164. [PubMed][CrossRef]
68. Dulebohn D, Choy J, Sundermeier T, Okan N, Karzai A. 2007. Trans-translation: the tmRNA-mediated surveillance mechanism for ribosome rescue, directed protein degradation, and nonstop mRNA decay. Biochemistry 46:4681–4693. [PubMed][CrossRef]
69. Shpanchenko O, Golovin A, Bugaeva E, Isaksson L, Dontsova O. 2010. Structural aspects of trans-translation. IUBMB Life 62:120–124. [PubMed]
70. Keiler KC, Waller PR, Sauer RT. 1996. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271:990–993. [PubMed][CrossRef]
71. Withey JH, Friedman DI. 2003. A salvage pathway for protein structures: tmRNA and trans-translation. Annu Rev Microbiol 57:101–123. [PubMed][CrossRef]
72. Williams KP, Bartel DP. 1996. Phylogenetic analysis of tmRNA secondary structure. RNA 2:1306–1310. [PubMed]
73. Felden B, Himeno H, Muto A, Atkins JF, Gesteland RF. 1996. Structural organization of Escherichia coli tmRNA. Biochimie 78:979–983. [PubMed][CrossRef]
74. Komine Y, Kitabatake M, Yokogawa T, Nishikawa K, Inokuchi H. 1994. A tRNA-like structure is present in 10Sa RNA, a small stable RNA from Escherichia coli. Proc Natl Acad Sci U S A 91:9223–9227. [PubMed][CrossRef]
75. Karzai AW, Roche ED, Sauer RT. 2000. The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue. Nat Struct Biol 7:449–455. [PubMed][CrossRef]
76. Babitzke P, Romeo T. 2007. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 10:156–163. [PubMed][CrossRef]
77. Timmermans J, Van Melderen L. 2010. Post-transcriptional global regulation by CsrA in bacteria. Cell Mol Life Sci 67:2897–2908. [PubMed][CrossRef]
78. Carmichael GG, Weber K, Niveleau A, Wahba AJ. 1975. The host factor required for RNA phage Qbeta RNA replication in vitro. Intracellular location, quantitation, and purification by polyadenylate-cellulose chromatography. J Biol Chem 250:3607–3612. [PubMed]
79. Kajitani M, Kato A, Wada A, Inokuchi Y, Ishihama A. 1994. Regulation of the Escherichia coli hfq gene encoding the host factor for phage Q beta. J Bacteriol 176:531–534. [PubMed]
80. Ali Azam T, Iwata A, Nishimura A, Ueda S, Ishihama A. 1999. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181:6361–6370. [PubMed]
81. Weichenrieder O. 2014. RNA binding by Hfq and ring-forming (L)Sm proteins: A trade-off between optimal sequence readout and RNA backbone conformation. RNA Biol 11(5):537–549. [PubMed][CrossRef]
82. Franze de Fernandez MT, Eoyang L, August JT. 1968. Factor fraction required for the synthesis of bacteriophage Qbeta-RNA. Nature 219:588–590. [PubMed][CrossRef]
83. Franze de Fernandez MT, Hayward WS, August JT. 1972. Bacterial proteins required for replication of phage Q ribonucleic acid. Pruification and properties of host factor I, a ribonucleic acid-binding protein. J Biol Chem 247:824–831. [PubMed]
84. Tsui HC, Leung HC, Winkler ME. 1994. Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol Microbiol 13:35–49. [PubMed][CrossRef]
85. Sittka A, Pfeiffer V, Tedin K, Vogel J. 2007. The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol Microbiol 63:193–217. [PubMed][CrossRef]
86. Hayashi-Nishino M, Fukushima A, Nishino K. 2012. Impact of hfq on the intrinsic drug resistance of Salmonella enterica serovar typhimurium. Front Microbiol 3:205. [PubMed][CrossRef]
87. 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. [PubMed][CrossRef]
88. Muffler A, Traulsen DD, Fischer D, Lange R, Hengge-Aronis R. 1997. The RNA-binding protein HF-I plays a global regulatory role which is largely, but not exclusively, due to its role in expression of the sigmaS subunit of RNA polymerase in Escherichia coli. J Bacteriol 179:297–300. [PubMed]
89. Tsui HC, Feng G, Winkler ME. 1997. Negative regulation of mutS and mutH repair gene expression by the Hfq and RpoS global regulators of Escherichia coli K-12. J Bacteriol 179:7476–7487. [PubMed]
90. Vytvytska O, Moll I, Kaberdin VR, von Gabain A, Blasi U. 2000. Hfq (HF1) stimulates ompA mRNA decay by interfering with ribosome binding. Genes Dev 14:1109–1118. [PubMed]
91. Vecerek B, Moll I, Blasi U. 2005. Translational autocontrol of the Escherichia coli hfq RNA chaperone gene. RNA 11:976–984. [PubMed][CrossRef]
92. Salvail H, Caron MP, Belanger J, Masse E. 2013. Antagonistic functions between the RNA chaperone Hfq and an sRNA regulate sensitivity to the antibiotic colicin. EMBO J 32:2764–2778. [PubMed][CrossRef]
93. Sauer E. 2013. Structure and RNA-binding properties of the bacterial LSm protein Hfq. RNA Biol 10:610–618. [PubMed][CrossRef]
94. Panja S, Woodson SA. 2012. Hexamer to monomer equilibrium of E. coli Hfq in solution and its impact on RNA annealing. J Mol Biol 417:406–412. [PubMed][CrossRef]
95. Link TM, Valentin-Hansen P, Brennan RG. 2009. Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc Natl Acad Sci U S A 106:19292–19297. [PubMed][CrossRef]
96. Mikulecky PJ, Kaw MK, Brescia CC, Takach JC, Sledjeski DD, Feig AL. 2004. Escherichia coli Hfq has distinct interaction surfaces for DsrA, rpoS and poly(A) RNAs. Nat Struct Mol Biol 11:1206–1214. [PubMed][CrossRef]
97. 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(19):3678–3697. [PubMed][CrossRef]
98. Sauer E, Schmidt S, Weichenrieder O. 2012. Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition. Proc Natl Acad Sci U S A 109:9396–9401. [PubMed][CrossRef]
99. Robinson KE, Orans J, Kovach AR, Link TM, Brennan RG. 2014. Mapping Hfq-RNA interaction surfaces using tryptophan fluorescence quenching. Nucleic Acids Res 42:2736–2749. [PubMed][CrossRef]
100. Valentin-Hansen P, Eriksen M, Udesen C. 2004. The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol Microbiol 51:1525–1533. [PubMed][CrossRef]
101. Ishikawa H, Otaka H, Maki K, Morita T, Aiba H. 2012. The functional Hfq-binding module of bacterial sRNAs consists of a double or single hairpin preceded by a U-rich sequence and followed by a 3′ poly(U) tail. RNA 18:1062–1074. [PubMed][CrossRef]
102. Otaka H, Ishikawa H, Morita T, Aiba H. 2011. PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action. Proc Natl Acad Sci U S A 108(32):13059–13064. [PubMed][CrossRef]
103. Soper TJ, Woodson SA. 2008. The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 14:1907–1917. [PubMed][CrossRef]
104. Salim NN, Faner MA, Philip JA, Feig AL. 2012. Requirement of upstream Hfq-binding (ARN)x elements in glmS and the Hfq C-terminal region for GlmS upregulation by sRNAs GlmZ and GlmY. Nucleic Acids Res 40:8021–8032. [PubMed][CrossRef]
105. Salim NN, Feig AL. 2010. An upstream Hfq binding site in the fhlA mRNA leader region facilitates the OxyS-fhlA interaction. PLoS One 5(9):e13028. [PubMed][CrossRef]
106. Sledjeski DD, Whitman C, Zhang A. 2001. Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 183:1997–2005. [PubMed][CrossRef]
107. Zhang A, Wassarman KM, Ortega J, Steven AC, Storz G. 2002. The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Molec Cell 9:11–22. [PubMed][CrossRef]
108. Fender A, Elf J, Hampel K, Zimmermann B, Wagner EG. 2010. RNAs actively cycle on the Sm-like protein Hfq. Genes Develop 24:2621–2626. [PubMed][CrossRef]
109. Hopkins JF, Panja S, Woodson SA. 2011. Rapid binding and release of Hfq from ternary complexes during RNA annealing. Nucleic Acids Res 39:5193–5202. [PubMed][CrossRef]
110. Maki K, Morita T, Otaka H, Aiba H. 2010. A minimal base-pairing region of a bacterial small RNA SgrS required for translational repression of ptsG mRNA. Molecular Microbiol 76:782–792. [PubMed][CrossRef]
111. 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 U S A 107:9602–9607. [PubMed][CrossRef]
112. Adamson DN, Lim HN. 2011. Essential requirements for robust signaling in Hfq dependent small RNA networks. PLoS Comput Biol 7:e1002138. [PubMed][CrossRef]
113. Hussein R, Lim HN. 2011. Disruption of small RNA signaling caused by competition for Hfq. Proc Natl Acad Sci U S A 108:1110–1115. [PubMed][CrossRef]
114. Moon K, Gottesman S. 2011. Competition among Hfq-binding small RNAs in Escherichia coli. Mol Microbiol 82:1545–1562. [PubMed][CrossRef]
115. Sukhodolets MV, Garges S. 2003. Interaction of Escherichia coli RNA polymerase with the ribosomal protein S1 and the Sm-like ATPase Hfq. Biochemistry 42:8022–8034. [PubMed][CrossRef]
116. Rabhi M, Espeli O, Schwartz A, Cayrol B, Rahmouni AR, Arluison V, Boudvillain M. 2011. The Sm-like RNA chaperone Hfq mediates transcription antitermination at Rho-dependent terminators. EMBO J 30:2805–2816. [PubMed][CrossRef]
117. Hajnsdorf E, Regnier P. 2000. Host factor Hfq of Escherichia coli stimulates elongation of poly(A) tails by poly(A) polymerase I. Proc Natl Acad Sci U S A 97:1501–1505. [PubMed][CrossRef]
118. Ikeda Y, Yagi M, Morita T, Aiba H. 2011. Hfq binding at RhlB-recognition region of RNase E is crucial for the rapid degradation of target mRNAs mediated by sRNAs in Escherichia coli. Mol Microbiol 79:419–432. [PubMed][CrossRef]
119. De Lay N, Gottesman S. 2011. Role of polynucleotide phosphorylase in sRNA function in Escherichia coli. RNA 17:1172–1189. [PubMed][CrossRef]
120. Mohanty BK, Maples VF, Kushner SR. 2004. The Sm-like protein Hfq regulates polyadenylation dependent mRNA decay in Escherichia coli. Mol Microbiol 54:905–920. [PubMed][CrossRef]
121. Bandyra KJ, Luisi BF. 2013. Licensing and due process in the turnover of bacterial RNA. RNA Biol 10:627–635. [PubMed][CrossRef]
122. Belasco JG. 2010. All things must pass: contrasts and commonalities in eukaryotic and bacterial mRNA decay. Nature reviews. Mol Cell Biol 11:467–478. [PubMed][CrossRef]
123. Carpousis AJ. 2007. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Ann Rev Microbiol 61:71–87. [PubMed][CrossRef]
124. Bandyra KJ, Said N, Pfeiffer V, Gorna 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. [PubMed][CrossRef]
125. Jiang X, Belasco JG. 2004. Catalytic activation of multimeric RNase E and RNase G by 5′-monophosphorylated RNA. Proc Natl Acad Sci U S A 101:9211–9216. [PubMed][CrossRef]
126. Dreyfus M. 2009. Killer and protective ribosomes. Prog Mol Biol Transl Sci 85:423–466. [PubMed]
127. Joyce SA, Dreyfus M. 1998. In the absence of translation, RNase E can bypass 5′ mRNA stabilizers in Escherichia coli. J Mol Biol 282:241–254. [PubMed][CrossRef]
128. Deana A, Belasco JG. 2005. Lost in translation: the influence of ribosomes on bacterial mRNA decay. Genes Dev 19:2526–2533. [PubMed][CrossRef]
129. Prevost K, Desnoyers G, Jacques JF, Lavoie F, Masse E. 2011. Small RNA-induced mRNA degradation achieved through both translation block and activated cleavage. Genes Dev 25:385–396. [PubMed][CrossRef]
130. Davies BW, Walker GC. 2008. A highly conserved protein of unknown function is required by Sinorhizobium meliloti for symbiosis and environmental stress protection. J Bacteriol 190:1118–1123. [PubMed][CrossRef]
131. Vercruysse M, Kohrer C, Davies BW, Arnold MF, Mekalanos JJ, RajBhandary UL, Walker GC. 2014. The Highly Conserved Bacterial RNase YbeY Is Essential in Vibrio cholerae, Playing a Critical Role in Virulence, Stress Regulation, and RNA Processing. PLoS Pathog 10:e1004175. [PubMed][CrossRef]
132. Meister G. 2013. Argonaute proteins: functional insights and emerging roles. Nat Rev Genet 14:447–459. [PubMed][CrossRef]
133. Jacob AI, Kohrer C, Davies BW, RajBhandary UL, Walker GC. 2013. Conserved bacterial RNase YbeY plays key roles in 70S ribosome quality control and 16S rRNA maturation. Mol Cell 49:427–438. [PubMed][CrossRef]
134. Davies BW, Kohrer C, Jacob AI, Simmons LA, Zhu J, Aleman LM, Rajbhandary UL, Walker GC. 2010. Role of Escherichia coli YbeY, a highly conserved protein, in rRNA processing. Mol Microbiol 78:506–518. [PubMed][CrossRef]
135. Pandey SP, Minesinger BK, Kumar J, Walker GC. 2011. A highly conserved protein of unknown function in Sinorhizobium meliloti affects sRNA regulation similar to Hfq. Nucleic Acids Res 39:4691–4708. [PubMed][CrossRef]
136. Pandey SP, Winkler JA, Li H, Camacho DM, Collins JJ, Walker GC. 2014. Central role for RNase YbeY in Hfq-dependent and Hfq-independent small-RNA regulation in bacteria. BMC Genomics 15:121. [PubMed][CrossRef]
137. Englesberg E, Anderson RL, Weinberg R, Lee N, Hoffee P, Huttenhauer G, Boyer H. 1962. L-Arabinose-sensitive, L-ribulose 5-phosphate 4-epimerase-deficient mutants of Escherichia coli. J Bacteriol 84:137–146. [PubMed]
138. Horler RS, Vanderpool CK. 2009. Homologs of the small RNA SgrS are broadly distributed in enteric bacteria but have diverged in size and sequence. Nucleic Acids Res 37:5465–5476. [PubMed][CrossRef]
139. Martinez-Hackert E, Stock AM. 1997. Structural relationships in the OmpR family of winged-helix transcription factors. J Mol Biol 269:301–312. [PubMed][CrossRef]
140. Tam R, Saier MH, Jr. 1993. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 57:320–346. [PubMed]
141. 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. [PubMed][CrossRef]
142. Kawamoto H, Koide Y, Morita T, Aiba H. 2006. Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol Microbiol 61:1013–1022. [PubMed][CrossRef]
143. Wadler C, Vanderpool C. 2007. A dual function for a bacterial small RNA: SgrS performs base pairing-dependent regulation and encodes a functional polypeptide. Proc Natl Acad Sci U S A 104:20454–20459. [PubMed][CrossRef]
144. Rice J, Vanderpool C. 2011. The small RNA SgrS controls sugar-phosphate accumulation by regulating multiple PTS genes. Nucleic Acids Res 39:3806–3819. [PubMed][CrossRef]
145. Rice JB, Balasubramanian D, Vanderpool CK. 2012. Small RNA binding-site multiplicity involved in translational regulation of a polycistronic mRNA. Proc Natl Acad Sci U S A 109:e2691–2698. [PubMed][CrossRef]
146. Richards GR, Vivas EI, Andersen AW, Rivera-Santos D, Gilmore S, Suen G, Goodrich-Blair H. 2009. Isolation and characterization of Xenorhabdus nematophila transposon insertion mutants defective in lipase activity against Tween. J Bacteriol 191:5325–5331. [PubMed][CrossRef]
147. 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 U S A 109:e757–764. [PubMed][CrossRef]
148. Jiang X, Rossanese OW, Brown NF, Kujat-Choy S, Galan JE, Finlay BB, Brumell JH. 2004. The related effector proteins SopD and SopD2 from Salmonella enterica serovar Typhimurium contribute to virulence during systemic infection of mice. Mol Microbiol 54:1186–1198. [PubMed][CrossRef]
149. Sun Y, Vanderpool CK. 2011. Regulation and function of Escherichia coli sugar efflux transporter A (SetA) during glucose-phosphate stress. J Bacteriol 193:143–153. [PubMed][CrossRef]
150. Liu JY, Miller PF, Willard J, Olson ER. 1999. Functional and biochemical characterization of Escherichia coli sugar efflux transporters. J Biol Chem 274:22977–22984. [PubMed][CrossRef]
151. Kim SH, Schneider BL, Reitzer L. 2010. Genetics and regulation of the major enzymes of alanine synthesis in Escherichia coli. J Bacteriol 192:5304–5311. [PubMed][CrossRef]
152. Vanderpool CK. 2007. Physiological consequences of small RNA-mediated regulation of glucose-phosphate stress. Curr Opin Microbiol 10:146–151. [PubMed][CrossRef]
153. Richards GR, Vanderpool CK. 2012. Induction of the Pho regulon suppresses the growth defect of an Escherichia coli sgrS mutant, connecting phosphate metabolism to the glucose-phosphate stress response. J Bacteriol 194:2520–2530. [PubMed][CrossRef]
154. Sun Y, Vanderpool CK. 2013. Physiological consequences of multiple-target regulation by the small RNA SgrS in Escherichia coli. J Bacteriol 195:4804–4815. [PubMed][CrossRef]
155. Horler R, Vanderpool C. 2009. Homologs of the small RNA SgrS are broadly distributed in enteric bacteria but have diverged in size and sequence. Nucleic Acids Res 37:5465–5476. [PubMed][CrossRef]
156. Wadler C, Vanderpool C. 2009. Characterization of homologs of the small RNA SgrS reveals diversity in function. Nucleic Acids Res 37:5477–5485. [PubMed][CrossRef]
157. Balasubramanian D, Vanderpool CK. 2013. Deciphering the interplay between two independent functions of the small RNA regulator SgrS in Salmonella. J Bacteriol 195:4620–4630. [PubMed][CrossRef]
158. Kimata K, Tanaka Y, Inada T, Aiba H. 2001. Expression of the glucose transporter gene, ptsG, is regulated at the mRNA degradation step in response to glycolytic flux in Escherichia coli. EMBO J 20:3587–3595. [PubMed][CrossRef]
159. Morita T, El-Kazzaz W, Tanaka Y, Inada T, Aiba H. 2003. Accumulation of glucose 6-phosphate or fructose 6-phosphate is responsible for destabilization of glucose transporter mRNA in Escherichia coli. J Biol Chem 278:15608–15614. [PubMed][CrossRef]
160. Richards GR, Patel MV, Lloyd CR, Vanderpool CK. 2013. Depletion of glycolytic intermediates plays a key role in glucose-phosphate stress in Escherichia coli. J Bacteriol 195:4816–4825. [PubMed][CrossRef]
161. Morita T, El-Kazzaz W, Tanaka Y, Inada T, Aiba H. 2003. Accumulation of glucose 6-phosphate or fructose 6-phosphate is responsible for destabilization of glucose transporter mRNA in Escherichia coli. J Biol Chem 278:15608–15614. [PubMed][CrossRef]
162. 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 Develop 16:1696–1706. [PubMed][CrossRef]
163. Adhya S. 1987. The galactose operon, p 1503–1512. In Neidhardt FC, Ingraham JL, Curtiss R (ed), Escherichia coli and Salmonella typhimurium: Cellular and molecular biology. ASM Press, Washington, D.C.
164. 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. [PubMed][CrossRef]
165. Rice PW, Dahlberg JE. 1982. A gene between polA and glnA retards growth of Escherichia coli when present in multiple copies: physiological effects of the gene for spot 42 RNA. J Bacteriol 152:1196–1210. [PubMed]
166. 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. [PubMed]
167. Sahagan B, Dahlberg JE. 1979. A small, unstable RNA molecule of Escherichia coli: Spot 42 RNA. J Mol Biol 131:593–605. [PubMed][CrossRef]
168. Joseph E, Danchin A, Ullmann A. 1981. Regulation of galactose operon expression: glucose effects and role of cyclic adenosine 3′,5′-monophosphate. J Bacteriol 146:149–154. [PubMed]
169. Queen C, Rosenberg M. 1981. Differential translation efficiency explains discoordinate expression of the galactose operon. Cell 25:241–249. [PubMed][CrossRef]
170. Sonnleitner E, Abdou L, Haas D. 2009. Small RNA as global regulator of carbon catabolite repression in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 106:21866–21871. [PubMed][CrossRef]
171. Liu P. 1952. Utilization of carbohydrates by Pseudomonas aeruginosa. J Bacteriol 64:773–781. [PubMed]
172. Smyth PF, Clarke PH. 1975. Catabolite repression of Pseudomonas aeruginosa amidase: The effect of carbon source on amidase synthesis. J Gen Microbiol 90:81–90. [PubMed][CrossRef]
173. Collier DN, Hager PW, Phibbs PV. 1996. Catabolite repression control in the pseudomonads. Res Microbiol 147:551–561. [PubMed][CrossRef]
174. Rojo F, Dinamarca MA. 2004. Catabolite repression and physiological control, p 365–387. In Ramos JL (ed), Pseudomonas: virulence and gene regulation, vol. 2. Kluwer Academic/Plenum, New York. [CrossRef]
175. MacGregor CH, Arora SK, Hager PW, Dail MB, Phibbs PVJ. 1996. The nucleotide sequence of the Pseudomonas aeruginosa pyrE-crc-rph region and the purification of the crc gene product. J Bacteriol 178:5627–5635. [PubMed]
176. MacGregor CH, Wolff JA, Arora SK, Phibbs PVJ. 1991. Cloning of a catabolite repression control (crc) gene from Pseudomonas aeruginosa, expression of the gene in Escherichia coli, and identification of the gene product in Pseudomonas aeruginosa. J Bacteriol 173:7204–7212. [PubMed]
177. Rojo F. 2010. Carbon catabolite repression in Pseudomonas: optimizing metabolic versatility and interactions with the environment. FEMS Microbiol Rev 34:658–684. [PubMed]
178. Moreno R, Martinez-Gomariz M, Yuste L, Gil C, Rojo F. 2009. The Pseudomonas putida Crc global regulator controls the hierarchical assimilation of amino acids in a complete medium: evidence from proteomic and genomic analyses. Proteomics 9:2910–2928. [PubMed][CrossRef]
179. Moreno R, Rojo F. 2008. The target for the Pseudomonas putida Crc global regulator in the benzoate degradation pathway is the BenR transcriptional regulator. J Bacteriol 190:1539–1545. [PubMed][CrossRef]
180. Moreno R, Ruiz-Manzano A, Yuste L, Rojo F. 2007. The Pseudomonas putida Crc global regulator is an RNA binding protein that inhibits translation of the AlkS transcriptional regulator. Mol Microbiol 64:665–675. [PubMed][CrossRef]
181. Milojevic T, Grishkovskaya I, Sonnleitner E, Djinovic-Carugo K, Bläsi U. 2013. The Pseudomonas aeruginosa catabolite repression control protein Crc is devoid of RNA binding activity. PLoS ONE 8:e64609. [PubMed][CrossRef]
182. Milojevic T, Sonnleitner E, Romeo A, Djinović-Carugo K, Bläsi U. 2013. False positive RNA binding activities after Ni-affinity purification from Escherichia coli. RNA Biol 10:1066–1069. [PubMed][CrossRef]
183. Sonnleitner E, Bläsi U. 2014. Regulation of Hfq by the RNA CrcZ in Pseudomonas aeruginosa carbon catabolite repression. PLoS Genet 10:e1004440. [PubMed][CrossRef]
184. Wolff JA, MacGregor CH, Eisenberg RC, Phibbs PV. 1991. Isolation and characterization of catabolite repression control mutants of Pseudomonas aeruginosa PAO. J Bacteriol 173:4700–4706. [PubMed]
185. Amador CI, Canosa I, Govantes F, Santero E. 2010. Lack of CbrB in Pseudomonas putida affects not only amino acids metabolism but also different stress responses and biofilm development. Environ Microbiol 12:1748–1761. [PubMed][CrossRef]
186. O'Toole GA, Gibbs KA, Hager PW, Phibbs PVJ, Kolter R. 2000. The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J Bacteriol 182:425–431. [PubMed][CrossRef]
187. Moreno R, Fonseca P, Rojo F. 2012. Two small RNAs, CrcY and CrcZ, act in concert to sequester the Crc global regulator in Pseudomonas putida, modulating catabolite repression. Mol Microbiol 83:24–40. [PubMed][CrossRef]
188. Filiatrault MJ, Stodghill PV, Wilson J, Butcher BG, Chen H, al. e. 2013. CrcZ and CrcX regulate carbon source utilization in Pseudomonas syringae pathovar tomato strain DC3000. RNA Biol 10:245–255. [PubMed][CrossRef]
189. Joanny G, Le Derout J, Brechemier-Baey D, Labas V, Vinh J, Régnier P, Hajnsdorf E. 2007. Polyadenylation of a functional mRNA controls gene expression in Escherichia coli. Nucleic Acids Res 35:2494–2502. [PubMed][CrossRef]
190. Kalamorz F, Reichenbach B, Marz W, Rak B, Gorke B. 2007. Feedback control of glucosamine-6-phosphate synthase GlmS expression depends on the small RNA GlmZ and involves the novel protein YhbJ in Escherichia coli. Mol Microbiol 65:1518–1533. [PubMed][CrossRef]
191. Reichenbach B, Maes A, Kalamorz F, Hajnsdorf E, Gorke B. 2008. The small RNA GlmY acts upstream of the sRNA GlmZ in the activation of glmS expression and is subject to regulation by polyadenylation in Escherichia coli. Nucleic Acids Res. 36:2570–2580. [PubMed][CrossRef]
192. Urban JH, Papenfort K, Thomsen J, Schmitz RA, Vogel J. 2007. A conserved small RNA promotes discoordinate expression of the glmUS operon mRNA to activate GlmS synthesis. Journal Mol Biol 373:521–528. [PubMed][CrossRef]
193. Urban JH, Vogel J. 2008. Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol 6:e64. [PubMed][CrossRef]
194. 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 Devel 27:552–564. [PubMed][CrossRef]
195. Urbanowski ML, Stauffer LT, Stauffer GV. 2000. The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport systems in Escherichia coli. Mol Microbiol 37:856–868. [PubMed][CrossRef]
196. Pulvermacher SC, Stauffer LT, Stauffer GV. 2008. The role of the small regulatory RNA GcvB in GcvB/mRNA posttranscriptional regulation of oppA and dppA in Escherichia coli. FEMS Microbiol Lett 281:42–50. [PubMed][CrossRef]
197. Pulvermacher SC, Stauffer LT, Stauffer GV. 2009. Role of the sRNA GcvB in regulation of cycA in Escherichia coli. Microbiology 155:106–114. [PubMed][CrossRef]
198. Stauffer LT, Stauffer GV. 2012. The Escherichia coli GcvB sRNA uses genetic redundancy to control cycA expression. ISRN Microbiol 2012. [PubMed][CrossRef]
199. Sharma C, Darfeuille F, Plantinga T, 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 Devel 21:2804–2817. [PubMed][CrossRef]
200. McArthur SD, Pulvermacher SC, Stauffer GV. 2006. The Yersinia pestis gcvB gene encodes two small regulatory RNA molecules. BMC Microbiol 6:52. [PubMed][CrossRef]
201. Silveira AC, Robertson KL, Lin B, Wang Z, Vora GJ, Vasconcelos AT, Thompson FL. 2010. Identification of non-coding RNAs in environmental vibrios. Microbiology 156:2452–2458. [PubMed][CrossRef]
202. 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(5):1144–1165. [PubMed][CrossRef]
203. 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. [PubMed][CrossRef]
204. Gerstle K, Klätschke K, Hahn U, Piganeau N. 2012. The small RNA RybA regulates key-genes in the biosynthesis of aromatic amino acids under peroxide stress in E. coli. RNA Biol 9:458–468. [PubMed][CrossRef]
205. Schilling D, Findeiss S, Richter AS, Taylor JA, Gerischer U. 2010. The small RNA Aar in Acinetobacter baylyi: a putative regulator of amino acid metabolism. Arch Microbiol 192:691–702. [PubMed][CrossRef]
206. Andrews SC, Robinson AK, Rodriguez-Quinones F. 2003. Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237. [PubMed][CrossRef]
207. Schaible UE, Kaufmann SH. 2004. Iron and microbial infection. Nat Rev Microbiol 2:946–953. [PubMed][CrossRef]
208. Masse E, Vanderpool CK, Gottesman S. 2005. Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol 187:6962–6971. [PubMed][CrossRef]
209. Geissmann, Touati D. 2004. Hfq, a new chaperoning role: binding to messanger RNA determines access for small RNA regulator. EMBO J 23:396–405. [PubMed][CrossRef]
210. Vecerek B, Moll I, Afonyushkin T, Kaberdin V, Blasi U. 2003. Interaction of the RNA chaperone Hfq with mRNAs: direct and indirect roles of Hfq in iron metabolism of Escherichia coli. Molec Microbiol 50:897–909. [PubMed][CrossRef]
211. Hantke K. 1981. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet 182:288–292. [PubMed][CrossRef]
212. Salvail H, Lanthier-Bourbonnais P, Sobota JM, Caza M, Benjamin JA, Mendieta ME, Lepine F, Dozois CM, Imlay J, Masse E. 2010. A small RNA promotes siderophore production through transcriptional and metabolic remodeling. Proc Natl Acad Sci U S A 107:15223–15228. [PubMed][CrossRef]
213. Ochsner UA, Wilderman PJ, Vasil AI, Vasil ML. 2002. GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol 45:1277–1287. [PubMed][CrossRef]
214. Wilderman PJ, Sowa NA, FitzGerald DJ, FitzGerald PC, Gottesman S, Ochsner UA, Vasil ML. 2004. Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc Natl Acad Sci U S A 101:9792–9797. [PubMed][CrossRef]
215. Oglesby-Sherrouse AG, Vasil ML. 2010. Characterization of a heme-regulated non-coding RNA encoded by the prrF locus of Pseudomonas aeruginosa. PLoS ONE 5:e9930. [PubMed][CrossRef]
216. Romeo T, Vakulskas CA, Babitzke P. 2013. Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. Environ Microbiol 15:313–324. [PubMed][CrossRef]
217. Wang X, Preston JF, 3rd, Romeo T. 2004. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol 186:2724–2734. [PubMed][CrossRef]
218. Itoh Y, Wang X, Hinnebusch BJ, Preston JF, 3rd, Romeo T. 2005. Depolymerization of beta-1,6-N-acetyl-D-glucosamine disrupts the integrity of diverse bacterial biofilms. J Bacteriol 187:382–387. [PubMed][CrossRef]
219. Jackson DW, Suzuki K, Oakford L, Simecka JW, Hart ME, Romeo T. 2002. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol 184:290–301. [PubMed][CrossRef]
220. Wang X, Dubey AK, Suzuki K, Baker CS, Babitzke P, Romeo T. 2005. CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol Microbiol 56:1648–1663. [PubMed][CrossRef]
221. Yakhnin H, Yakhnin AV, Baker CS, Sineva E, Berezin I, Romeo T, Babitzke P. 2011. Complex regulation of the global regulatory gene csrA: CsrA-mediated translational repression, transcription from five promoters by Esigma(7)(0) and Esigma(S), and indirect transcriptional activation by CsrA. Mol Microbiol 81:689–704. [PubMed][CrossRef]
222. Wei BL, Brun-Zinkernagel AM, Simecka JW, Pruss BM, Babitzke P, Romeo T. 2001. Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 40:245–256. [PubMed][CrossRef]
223. Yakhnin AV, Baker CS, Vakulskas CA, Yakhnin H, Berezin I, Romeo T, Babitzke P. 2013. CsrA activates flhDC expression by protecting flhDC mRNA from RNase E-mediated cleavage. Mol Microbiol 87:851–866. [PubMed][CrossRef]
224. Mercante J, Edwards AN, Dubey AK, Babitzke P, Romeo T. 2009. Molecular geometry of CsrA (RsmA) binding to RNA and its implications for regulated expression. J Mol Biol 392:511–528. [PubMed][CrossRef]
225. Dubey AK, Baker CS, Romeo T, Babitzke P. 2005. RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA 11:1579–1587. [PubMed][CrossRef]
226. Schubert M, Lapouge K, Duss O, Oberstrass FC, Jelesarov I, Haas D, Allain FH. 2007. Molecular basis of messenger RNA recognition by the specific bacterial repressing clamp RsmA/CsrA. Nat Struct Mol Biol 14:807–813. [PubMed][CrossRef]
227. Liu MY, Gui G, Wei B, Preston JF, 3rd, Oakford L, Yuksel U, Giedroc DP, Romeo T. 1997. The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J Biol Chem 272:17502–17510. [PubMed][CrossRef]
228. Weilbacher T, Suzuki K, Dubey AK, Wang X, Gudapaty S, Morozov I, Baker CS, Georgellis D, Babitzke P, Romeo T. 2003. A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol Microbiol 48:657–670. [PubMed][CrossRef]
229. Chavez RG, Alvarez AF, Romeo T, Georgellis D. 2010. The physiological stimulus for the BarA sensor kinase. J Bacteriol 192:2009–2012. [PubMed][CrossRef]
230. Suzuki K, Wang X, Weilbacher T, Pernestig AK, Melefors O, Georgellis D, Babitzke P, Romeo T. 2002. Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol 184:5130–5140. [PubMed][CrossRef]
231. 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. [PubMed][CrossRef]
232. Fields JA, Thompson SA. 2008. Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. J Bacteriol 190:3411–3416. [PubMed][CrossRef]
233. Jonas K, Edwards AN, Ahmad I, Romeo T, Romling U, Melefors O. 2010. Complex regulatory network encompassing the Csr, c-di-GMP and motility systems of Salmonella Typhimurium. Environ Microbiol 12:524–540. [PubMed][CrossRef]
234. Jones MK, Warner EB, Oliver JD. 2008. csrA inhibits the formation of biofilms by Vibrio vulnificus. Appl Environ Microbiol 74:7064–7066. [PubMed][CrossRef]
235. Blumer C, Haas D. 2000. Iron regulation of the hcnABC genes encoding hydrogen cyanide synthase depends on the anaerobic regulator ANR rather than on the global activator GacA in Pseudomonas fluorescens CHA0. Microbiology 146(Pt 10):2417–2424. [PubMed]
236. Kay E, Dubuis C, Haas D. 2005. Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc Natl Acad Sci U S A 102:17136–17141. [PubMed][CrossRef]
237. Moll S, Schneider DJ, Stodghill P, Myers CR, Cartinhour SW, Filiatrault MJ. 2010. Construction of an rsmX co-variance model and identification of five rsmX non-coding RNAs in Pseudomonas syringae pv. tomato DC3000. RNA Biol 7:508–516. [CrossRef]
238. Heeb S, Blumer C, Haas D. 2002. Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J Bacteriol 184:1046–1056. [PubMed][CrossRef]
239. Valverde C, Heeb S, Keel C, Haas D. 2003. RsmY, a small regulatory RNA, is required in concert with RsmZ for GacA-dependent expression of biocontrol traits in Pseudomonas fluorescens CHA0. Mol Microbiol 50:1361–1379. [PubMed][CrossRef]
240. Laville J, Voisard C, Keel C, Maurhofer M, Defago G, Haas D. 1992. Global control in Pseudomonas fluorescens mediating antibiotic synthesis and suppression of black root rot of tobacco. Proc Natl Acad Sci U S A 89:1562–1566. [PubMed][CrossRef]
241. Zuber S, Carruthers F, Keel C, Mattart A, Blumer C, Pessi G, Gigot-Bonnefoy C, Schnider-Keel U, Heeb S, Reimmann C, Haas D. 2003. GacS sensor domains pertinent to the regulation of exoproduct formation and to the biocontrol potential of Pseudomonas fluorescens CHA0. Mol Plant Microbe Interact 16:634–644. [PubMed][CrossRef]
242. Jorgensen 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. [PubMed][CrossRef]
243. 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. [PubMed][CrossRef]
244. Hammar M, Arnqvist A, Bian Z, Olsen A, Normark S. 1995. Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 18:661–670. [PubMed][CrossRef]
245. Pesavento C, Becker G, Sommerfeldt N, Possling A, Tschowri N, Mehlis A, Hengge R. 2008. Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes Dev 22:2434–2446. [PubMed][CrossRef]
246. Zogaj X, Nimtz M, Rohde M, Bokranz W, Romling U. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39:1452–1463. [PubMed][CrossRef]
247. Ogasawara H, Yamamoto K, Ishihama A. 2011. Role of the biofilm master regulator CsgD in cross-regulation between biofilm formation and flagellar synthesis. J Bacteriol 193:2587–2597. [PubMed][CrossRef]
248. Wolfe AJ, Visick KL. 2008. Get the message out: cyclic-Di-GMP regulates multiple levels of flagellum-based motility. J Bacteriol 190:463–475. [PubMed][CrossRef]
249. De Lay N, Gottesman S. 2012. A complex network of small non-coding RNAs regulate motility in Escherichia coli. Mol Microbiol 86:524–538. [PubMed][CrossRef]
250. Guillier M, Gottesman S. 2006. Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol Microbiol 59:231–247. [PubMed][CrossRef]
251. 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. [PubMed][CrossRef]
252. 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. [PubMed][CrossRef]
253. Redfield RJ. 2002. Is quorum sensing a side effect of diffusion sensing? Trends Microbiol 10:365–370. [PubMed][CrossRef]
254. West SA, Winzer K, Gardner A, Diggle SP. 2012. Quorum sensing and the confusion about diffusion. Trends Microbiol 20:586–594. [PubMed][CrossRef]
255. Ng WL, Bassler BL. 2009. Bacterial quorum-sensing network architectures. Ann Rev Genet 43:197–222. [PubMed][CrossRef]
256. Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Ann Rev Cell Devel Bio 21:319–346. [PubMed][CrossRef]
257. Rutherford ST, Bassler BL. 2012. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2(11):a012427. [PubMed][CrossRef]
258. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL. 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:69–82. [PubMed][CrossRef]
259. Bardill JP, Zhao X, Hammer BK. 2011. The Vibrio cholerae quorum sensing response is mediated by Hfq-dependent sRNA/mRNA base pairing interactions. Mol Microbiol 80:1381–1394. [PubMed][CrossRef]
260. Rutherford ST, van Kessel JC, Shao Y, Bassler BL. 2011. AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev 25:397–408. [PubMed][CrossRef]
261. Shao Y, Bassler BL. 2012. Quorum-sensing non-coding small RNAs use unique pairing regions to differentially control mRNA targets. Mol Microbiol 83:599–611. [PubMed][CrossRef]
262. Tu KC, Bassler BL. 2007. Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev 21:221–233. [PubMed][CrossRef]
263. Shao Y, Bassler BL. 2014. Quorum regulatory small RNAs repress type VI secretion in Vibrio cholerae. Mol Microbiol 92:921–930. [PubMed][CrossRef]
264. Svenningsen SL, Tu KC, Bassler BL. 2009. Gene dosage compensation calibrates four regulatory RNAs to control Vibrio cholerae quorum sensing. EMBO J 28:429–439. [PubMed][CrossRef]
265. Lin W, Kovacikova G, Skorupski K. 2005. Requirements for Vibrio cholerae HapR binding and transcriptional repression at the hapR promoter are distinct from those at the aphA promoter. J Bacteriol 187:3013–3019. [PubMed][CrossRef]
266. Svenningsen SL, Waters CM, Bassler BL. 2008. A negative feedback loop involving small RNAs accelerates Vibrio cholerae's transition out of quorum-sensing mode. Genes Dev 22:226–238. [PubMed][CrossRef]
267. Lee YH, Kim S, Helmann JD, Kim BH, Park YK. 2013. RaoN, a small RNA encoded within Salmonella pathogenicity island-11, confers resistance to macrophage-induced stress. Microbiology 159:1366–1378. [PubMed][CrossRef]
268. de Jong HK, Parry CM, van der Poll T, Wiersinga WJ. 2012. Host-pathogen interaction in invasive Salmonellosis. PLoS Pathog 8:e1002933. [PubMed][CrossRef]
269. Fabrega A, Vila J. 2013. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev 26:308–341. [PubMed][CrossRef]
270. Sabbagh SC, Forest CG, Lepage C, Leclerc JM, Daigle F. 2010. So similar, yet so different: uncovering distinctive features in the genomes of Salmonella enterica serovars Typhimurium and Typhi. FEMS Microbiol Lett 305:1–13. [PubMed][CrossRef]
271. Gunn JS, Alpuche-Aranda CM, Loomis WP, Belden WJ, Miller SI. 1995. Characterization of the Salmonella typhimurium pagC/pagD chromosomal region. J Bacteriol 177:5040–5047. [PubMed]
272. Miller SI, Kukral AM, Mekalanos JJ. 1989. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci U S A 86:5054–5058. [PubMed][CrossRef]
273. 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. Bio Systems 65:157–177. [PubMed][CrossRef]
274. 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. [PubMed][CrossRef]
275. Tramonti A, De Canio M, De Biase D. 2008. GadX/GadW-dependent regulation of the Escherichia coli acid fitness island: transcriptional control at the gadY-gadW divergent promoters and identification of four novel 42 bp GadX/GadW-specific binding sites. Mol Microbiol 70:965–982. [PubMed]
276. Giannella RA, Broitman SA, Zamcheck N. 1972. Gastric acid barrier to ingested microorganisms in man: studies in vivo and in vitro. Gut 13:251–256. [PubMed][CrossRef]
277. Giannella RA, Broitman SA, Zamcheck N. 1973. Influence of gastric acidity on bacterial and parasitic enteric infections. A perspective. Ann Intern Med 78:271–276. [PubMed][CrossRef]
278. Arnold KW, Kaspar CW. 1995. Starvation- and stationary-phase-induced acid tolerance in Escherichia coli O157:H7. Appl Environ Microbiol 61:2037–2039. [PubMed]
279. Benjamin MM, Datta AR. 1995. Acid tolerance of enterohemorrhagic Escherichia coli. Appl Environ Microbiol 61:1669–1672. [PubMed]
280. Conner DE, Kotrola JS. 1995. Growth and survival of Escherichia coli O157:H7 under acidic conditions. Appl Environ Microbiol 61:382–385. [PubMed]
281. Ma Z, Gong S, Richard H, Tucker DL, Conway T, Foster JW. 2003. GadE (YhiE) activates glutamate decarboxylase-dependent acid resistance in Escherichia coli K-12. Mol Microbiol 49:1309–1320. [PubMed][CrossRef]
282. Ma Z, Richard H, Tucker DL, Conway T, Foster JW. 2002. Collaborative regulation of Escherichia coli glutamate-dependent acid resistance by two AraC-like regulators, GadX and GadW (YhiW). J Bacteriol 184:7001–7012. [PubMed][CrossRef]
283. Tramonti A, De Canio M, Delany I, Scarlato V, De Biase D. 2006. Mechanisms of transcription activation exerted by GadX and GadW at the gadA and gadBC gene promoters of the glutamate-based acid resistance system in Escherichia coli. J Bacteriol 188:8118–8127. [PubMed][CrossRef]
284. Takada A, Umitsuki G, Nagai K, Wachi M. 2007. RNase E is required for induction of the glutamate-dependent acid resistance system in Escherichia coli. Biosci Biotechnol Biochem 71:158–164. [PubMed][CrossRef]
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/content/journal/microbiolspec/10.1128/microbiolspec.MBP-0009-2014
2015-06-18
2017-09-21

Abstract:

Over the last decade, small (often noncoding) RNA molecules have been discovered as important regulators influencing myriad aspects of bacterial physiology and virulence. In particular, small RNAs (sRNAs) have been implicated in control of both primary and secondary metabolic pathways in many bacterial species. This chapter describes characteristics of the major classes of sRNA regulators, and highlights what is known regarding their mechanisms of action. Specific examples of sRNAs that regulate metabolism in gram-negative bacteria are discussed, with a focus on those that regulate gene expression by base pairing with mRNA targets to control their translation and stability.

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FIGURE 1

Simplified network of sRNAs regulating biofilm formation and motility in . The regulatory network shows a set of sRNAs (in bold) and relevant protein factors (grey boxes) controlling (blue circle), (red circle) and (violet circle) at the transcriptional (dashed lines), translational (solid lines) and protein (dotted lines) levels. Other factors known to regulate , , and were omitted for clarity. Arrows indicate activating interactions, and lines with blunt ends indicate inhibitory interactions. doi:10.1128/microbiolspec.MBP-0009-2014.f1

Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.MBP-0009-2014
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FIGURE 2

Quorum sensing systems of . uses histidine kinases CqsS and LuxPQ to sense autoinducers (AIs) CAI-1 (violet triangle) and AI-2 (orange triangle) respectively. Receptors function as kinases at low cell density (LCD), when concentrations of CAI-1 and AI-2, which are produced by CqsA and LuxS, respectively, are low. This stimulates σ-dependent activation of gene expression through LuxU and LuxO phosphorylation cascade. The Qrr 1-4 sRNAs (red square), facilitated by Hfq, activate , which stimulates expression of , a known activator of the major virulence factors. Additionally Qrr 1-4 repress , which leads to polysaccharide production and biofilm formation. Qrr 1-4 also negatively regulate genes for biogenesis of type VI secretion system (T6SS). In contrast, at high cell density (HCD) receptors sense the presence of AIs and function as phosphatases that stimulate dephosphorylation of LuxU, resulting in cessation of expression. In the absence of Qrr sRNAs, expression increases, which leads to the inhibition of biofilm formation and shut down of virulence factor production, while stimulating T6SS biosynthesis. Lines with arrowheads indicate activating interactions, and lines with blunt ends indicate inhibitory interactions. doi:10.1128/microbiolspec.MBP-0009-2014.f2

Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.MBP-0009-2014
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