1887

Abstract

Unlike proteins, RNA molecules have emerged lately as key players in regulation in bacteria. Most reviews hitherto focused on the experimental and/or methods used to identify genes encoding small RNAs (sRNAs) or on the diverse mechanisms of these RNA regulators to modulate expression of their targets. However, less is known about their biological functions and their implications in various physiological responses. This review aims to compile what is known presently about the diverse roles of sRNA transcripts in the regulation of metabolic processes, in different growth conditions, in adaptation to stress and in microbial pathogenesis. Several recent studies revealed that sRNA molecules are implicated in carbon metabolism and transport, amino acid metabolism or metal sensing. Moreover, regulatory RNAs participate in cellular adaptation to environmental changes, e.g. through quorum sensing systems or development of biofilms, and analyses of several sRNAs under various physiological stresses and culture conditions have already been performed. In addition, recent experiments performed with Gram-positive and Gram-negative pathogens showed that regulatory RNAs play important roles in microbial virulence and during infection. The combined results show the diversity of regulation mechanisms and physiological processes in which sRNA molecules are key actors.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.076208-0
2014-06-01
2019-12-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/6/1007.html?itemId=/content/journal/micro/10.1099/mic.0.076208-0&mimeType=html&fmt=ahah

References

  1. Aiba H.. ( 2007;). Mechanism of RNA silencing by Hfq-binding small RNAs. . Curr Opin Microbiol 10:, 134–139. [CrossRef][PubMed]
    [Google Scholar]
  2. Altuvia S.. ( 2007;). Identification of bacterial small non-coding RNAs: experimental approaches. . Curr Opin Microbiol 10:, 257–261. [CrossRef][PubMed]
    [Google Scholar]
  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. [CrossRef][PubMed]
    [Google Scholar]
  4. Altuvia S., Zhang A., Argaman L., Tiwari A., Storz G.. ( 1998;). The Escherichia coli OxyS regulatory RNA represses fhlA translation by blocking ribosome binding. . EMBO J 17:, 6069–6075. [CrossRef][PubMed]
    [Google Scholar]
  5. Andersen J., Delihas N.. ( 1990;). micF RNA binds to the 5′ end of ompF mRNA and to a protein from Escherichia coli. . Biochemistry 29:, 9249–9256. [CrossRef][PubMed]
    [Google Scholar]
  6. Awad M. M., Ellemor D. M., Bryant A. E., Matsushita O., Boyd R. L., Stevens D. L., Emmins J. J., Rood J. I.. ( 2000;). Construction and virulence testing of a collagenase mutant of Clostridium perfringens. . Microb Pathog 28:, 107–117. [CrossRef][PubMed]
    [Google Scholar]
  7. Babitzke P., Romeo T.. ( 2007;). CsrB sRNA family: sequestration of RNA-binding regulatory proteins. . Curr Opin Microbiol 10:, 156–163. [CrossRef][PubMed]
    [Google Scholar]
  8. Bardill J. P., Zhao X., Hammer B. K.. ( 2011;). The Vibrio cholerae quorum sensing response is mediated by Hfq-dependent sRNA/mRNA base pairing interactions. . Mol Microbiol 80:, 1381–1394. [CrossRef][PubMed]
    [Google Scholar]
  9. Barrangou R.. ( 2013;). CRISPR–Cas systems and RNA-guided interference. . Wiley Interdiscip Rev RNA 4:, 267–278. [CrossRef][PubMed]
    [Google Scholar]
  10. Bassler B. L., Wright M., Silverman M. R.. ( 1994;). Sequence and function of LuxO, a negative regulator of luminescence in Vibrio harveyi. . Mol Microbiol 12:, 403–412. [CrossRef][PubMed]
    [Google Scholar]
  11. Beisel C. L., 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. [CrossRef][PubMed]
    [Google Scholar]
  12. Beisel C. L., Updegrove T. B., Janson B. J., Storz G.. ( 2012;). Multiple factors dictate target selection by Hfq-binding small RNAs. . EMBO J 31:, 1961–1974. [CrossRef][PubMed]
    [Google Scholar]
  13. Boisset S., Geissmann T., Huntzinger E., Fechter P., Bendridi N., Possedko M., Chevalier C., Helfer A. C., Benito Y.. & other authors ( 2007;). Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. . Genes Dev 21:, 1353–1366. [CrossRef][PubMed]
    [Google Scholar]
  14. Bordi C., Lamy M.-C., Ventre I., Termine E., Hachani A., Fillet S., Roche B., Bleves S., Méjean V.. & other authors ( 2010;). Regulatory RNAs and the HptB/RetS signalling pathways fine-tune Pseudomonas aeruginosa pathogenesis. . Mol Microbiol 76:, 1427–1443. [CrossRef][PubMed]
    [Google Scholar]
  15. Bradley E. S., Bodi K., Ismail A. M., Camilli A.. ( 2011;). A genome-wide approach to discovery of small RNAs involved in regulation of virulence in Vibrio cholerae. . PLoS Pathog 7:, e1002126. [CrossRef][PubMed]
    [Google Scholar]
  16. Brantl S.. ( 2007;). Regulatory mechanisms employed by cis-encoded antisense RNAs. . Curr Opin Microbiol 10:, 102–109. [CrossRef][PubMed]
    [Google Scholar]
  17. Castanie-Cornet M. P., Penfound T. A., Smith D., Elliott J. F., Foster J. W.. ( 1999;). Control of acid resistance in Escherichia coli. . J Bacteriol 181:, 3525–3535.[PubMed]
    [Google Scholar]
  18. Cheung A. L., Eberhardt K. J., Chung E., Yeaman M. R., Sullam P. M., Ramos M., Bayer A. S.. ( 1994;). Diminished virulence of a sar/agr mutant of Staphylococcus aureus in the rabbit model of endocarditis. . J Clin Invest 94:, 1815–1822. [CrossRef][PubMed]
    [Google Scholar]
  19. Constantinidou C., Hobman J. L., Griffiths L., Patel M. D., Penn C. W., Cole J. A., Overton T. W.. ( 2006;). A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth. . J Biol Chem 281:, 4802–4815. [CrossRef][PubMed]
    [Google Scholar]
  20. Coyer J., Andersen J., Forst S. A., Inouye M., Delihas N.. ( 1990;). micF RNA in ompB mutants of Escherichia coli: different pathways regulate micF RNA levels in response to osmolarity and temperature change. . J Bacteriol 172:, 4143–4150.[PubMed]
    [Google Scholar]
  21. De Lay N., Gottesman S.. ( 2012;). A complex network of small non-coding RNAs regulate motility in Escherichia coli. . Mol Microbiol 86:, 524–538. [CrossRef][PubMed]
    [Google Scholar]
  22. Deutscher J., Francke C., Postma P. W.. ( 2006;). How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. . Microbiol Mol Biol Rev 70:, 939–1031. [CrossRef][PubMed]
    [Google Scholar]
  23. Durand S., Storz G.. ( 2010;). Reprogramming of anaerobic metabolism by the FnrS small RNA. . Mol Microbiol 75:, 1215–1231. [CrossRef][PubMed]
    [Google Scholar]
  24. Ferrara S., Brugnoli M., De Bonis A., Righetti F., Delvillani F., Dehò G., Horner D., Briani F., Bertoni G.. ( 2012;). Comparative profiling of Pseudomonas aeruginosa strains reveals differential expression of novel unique and conserved small RNAs. . PLoS ONE 7:, e36553. [CrossRef][PubMed]
    [Google Scholar]
  25. Flemming H.-C., Wingender J.. ( 2010;). The biofilm matrix. . Nat Rev Microbiol 8:, 623–633.[PubMed]
    [Google Scholar]
  26. Fozo E. M., Hemm M. R., Storz G.. ( 2008;). Small toxic proteins and the antisense RNAs that repress them. . Microbiol Mol Biol Rev 72:, 579–589. [CrossRef][PubMed]
    [Google Scholar]
  27. Freeman J. A., Bassler B. L.. ( 1999;). A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi. . Mol Microbiol 31:, 665–677. [CrossRef][PubMed]
    [Google Scholar]
  28. Gardan R., Rapoport G., Débarbouillé M.. ( 1997;). Role of the transcriptional activator RocR in the arginine-degradation pathway of Bacillus subtilis. . Mol Microbiol 24:, 825–837. [CrossRef][PubMed]
    [Google Scholar]
  29. Georgellis D., Kwon O., Lin E. C.. ( 2001;). Quinones as the redox signal for the Arc two-component system of bacteria. . Science 292:, 2314–2316. [CrossRef][PubMed]
    [Google Scholar]
  30. Gillaspy A. F., Hickmon S. G., Skinner R. A., Thomas J. R., Nelson C. L., Smeltzer M. S.. ( 1995;). Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. . Infect Immun 63:, 3373–3380.[PubMed]
    [Google Scholar]
  31. Gong H., Vu G.-P., Bai Y., Chan E., Wu R., Yang E., Liu F., Lu S.. ( 2011;). A Salmonella small non-coding RNA facilitates bacterial invasion and intracellular replication by modulating the expression of virulence factors. . PLoS Pathog 7:, e1002120. [CrossRef][PubMed]
    [Google Scholar]
  32. González N., Heeb S., Valverde C., Kay E., Reimmann C., Junier T., Haas D.. ( 2008;). Genome-wide search reveals a novel GacA-regulated small RNA in Pseudomonas species. . BMC Genomics 9:, 167. [CrossRef][PubMed]
    [Google Scholar]
  33. Gottesman S.. ( 2005;). Micros for microbes: non-coding regulatory RNAs in bacteria. . Trends Genet 21:, 399–404. [CrossRef][PubMed]
    [Google Scholar]
  34. Gottesman S., Storz G.. ( 2011;). Bacterial small RNA regulators: versatile roles and rapidly evolving variations. . Cold Spring Harb Perspect Biol 3:, a003798. [CrossRef][PubMed]
    [Google Scholar]
  35. Grieshaber N. A., Grieshaber S. S., Fischer E. R., Hackstadt T.. ( 2006;). A small RNA inhibits translation of the histone-like protein Hc1 in Chlamydia trachomatis. . Mol Microbiol 59:, 541–550. [CrossRef][PubMed]
    [Google Scholar]
  36. Guillier M., Gottesman S., Storz G.. ( 2006;). Modulating the outer membrane with small RNAs. . Genes Dev 20:, 2338–2348. [CrossRef][PubMed]
    [Google Scholar]
  37. Hammer B. K., Bassler B. L.. ( 2007;). Regulatory small RNAs circumvent the conventional quorum sensing pathway in pandemic Vibrio cholerae. . Proc Natl Acad Sci U S A 104:, 11145–11149. [CrossRef][PubMed]
    [Google Scholar]
  38. Heidrich N., Chinali A., Gerth U., Brantl S.. ( 2006;). The small untranslated RNA SR1 from the Bacillus subtilis genome is involved in the regulation of arginine catabolism. . Mol Microbiol 62:, 520–536. [CrossRef][PubMed]
    [Google Scholar]
  39. Heidrich N., Moll I., Brantl S.. ( 2007;). In vitro analysis of the interaction between the small RNA SR1 and its primary target ahrC mRNA. . Nucleic Acids Res 35:, 4331–4346. [CrossRef][PubMed]
    [Google Scholar]
  40. Heroven A. K., Böhme K., Dersch P.. ( 2012;). The Csr/Rsm system of Yersinia and related pathogens: a post-transcriptional strategy for managing virulence. . RNA Biol 9:, 379–391. [CrossRef][PubMed]
    [Google Scholar]
  41. Hershberg R., Altuvia S., Margalit H.. ( 2003;). A survey of small RNA-encoding genes in Escherichia coli. . Nucleic Acids Res 31:, 1813–1820. [CrossRef][PubMed]
    [Google Scholar]
  42. Herskovits A. A., Bochkareva E. S., Bibi E.. ( 2000;). New prospects in studying the bacterial signal recognition particle pathway. . Mol Microbiol 38:, 927–939. [CrossRef][PubMed]
    [Google Scholar]
  43. Heurlier K., Williams F., Heeb S., Dormond C., Pessi G., Singer D., Cámara M., Williams P., Haas D.. ( 2004;). Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. . J Bacteriol 186:, 2936–2945. [CrossRef][PubMed]
    [Google Scholar]
  44. Hobbs E. C., Astarita J. L., Storz G.. ( 2010;). Small RNAs and small proteins involved in resistance to cell envelope stress and acid shock in Escherichia coli: analysis of a bar-coded mutant collection. . J Bacteriol 192:, 59–67. [CrossRef][PubMed]
    [Google Scholar]
  45. Homola A. D., Dekker E. E.. ( 1967;). Decarboxylation of γ-hydroxyglutamate by glutamate decarboxylase of Escherichia coli (ATCC 11246). . Biochemistry 6:, 2626–2634. [CrossRef][PubMed]
    [Google Scholar]
  46. Huntzinger E., Boisset S., Saveanu C., Benito Y., Geissmann T., Namane A., Lina G., Etienne J., Ehresmann B.. & other authors ( 2005;). Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. . EMBO J 24:, 824–835. [CrossRef][PubMed]
    [Google Scholar]
  47. Jacques J.-F., 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. [CrossRef][PubMed]
    [Google Scholar]
  48. Jin Y., Watt R. M., Danchin A., Huang J. D.. ( 2009;). Small noncoding RNA GcvB is a novel regulator of acid resistance in Escherichia coli. . BMC Genomics 10:, 165. [CrossRef][PubMed]
    [Google Scholar]
  49. Johansson J., Cossart P.. ( 2003;). RNA-mediated control of virulence gene expression in bacterial pathogens. . Trends Microbiol 11:, 280–285. [CrossRef][PubMed]
    [Google Scholar]
  50. Johnson J. R., Clabots C., Rosen H.. ( 2006;). Effect of inactivation of the global oxidative stress regulator oxyR on the colonization ability of Escherichia coli O1 : K1 : H7 in a mouse model of ascending urinary tract infection. . Infect Immun 74:, 461–468. [CrossRef][PubMed]
    [Google Scholar]
  51. Jørgensen M. G., Thomason M. K., Havelund J., Valentin-Hansen P., Storz G.. ( 2013;). Dual function of the McaS small RNA in controlling biofilm formation. . Genes Dev 27:, 1132–1145. [CrossRef][PubMed]
    [Google Scholar]
  52. Kang Y., Weber K. D., Qiu Y., Kiley P. J., Blattner F. R.. ( 2005;). Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. . J Bacteriol 187:, 1135–1160. [CrossRef][PubMed]
    [Google Scholar]
  53. Kay E., Humair B., Dénervaud V., Riedel K., Spahr S., Eberl L., Valverde C., Haas D.. ( 2006;). Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. . J Bacteriol 188:, 6026–6033. [CrossRef][PubMed]
    [Google Scholar]
  54. Kim Y.-M., Ogawa W., Tamai E., Kuroda T., Mizushima T., Tsuchiya T.. ( 2002;). Purification, reconstitution, and characterization of Na+/serine symporter, SstT, of Escherichia coli. . J Biochem 132:, 71–76. [CrossRef][PubMed]
    [Google Scholar]
  55. Kint G., De Coster D., Marchal K., Vanderleyden J., De Keersmaecker S. C. J.. ( 2010;). The small regulatory RNA molecule MicA is involved in Salmonella enterica serovar Typhimurium biofilm formation. . BMC Microbiol 10:, 276. [CrossRef][PubMed]
    [Google Scholar]
  56. Klenk M., Koczan D., Guthke R., Nakata M., Thiesen H.-J., Podbielski A., Kreikemeyer B.. ( 2005;). Global epithelial cell transcriptional responses reveal Streptococcus pyogenes Fas regulator activity association with bacterial aggressiveness. . Cell Microbiol 7:, 1237–1250. [CrossRef][PubMed]
    [Google Scholar]
  57. Koo J. T., Alleyne T. M., Schiano C. A., Jafari N., Lathem W. W.. ( 2011;). Global discovery of small RNAs in Yersinia pseudotuberculosis identifies Yersinia-specific small, noncoding RNAs required for virulence. . Proc Natl Acad Sci U S A 108:, E709–E717. [CrossRef][PubMed]
    [Google Scholar]
  58. Korem M., Gov Y., Kiran M. D., Balaban N.. ( 2005;). Transcriptional profiling of target of RNAIII-activating protein, a master regulator of staphylococcal virulence. . Infect Immun 73:, 6220–6228. [CrossRef][PubMed]
    [Google Scholar]
  59. Kreikemeyer B., Boyle M. D., Buttaro B. A., Heinemann M., Podbielski A.. ( 2001;). Group A streptococcal growth phase-associated virulence factor regulation by a novel operon (Fas) with homologies to two-component-type regulators requires a small RNA molecule. . Mol Microbiol 39:, 392–406. [CrossRef][PubMed]
    [Google Scholar]
  60. Lai L. B., Vioque A., Kirsebom L. A., Gopalan V.. ( 2010;). Unexpected diversity of RNase P, an ancient tRNA processing enzyme: challenges and prospects. . FEBS Lett 584:, 287–296. [CrossRef][PubMed]
    [Google Scholar]
  61. Lapouge K., Schubert M., Allain F. H.-T., Haas D.. ( 2008;). Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. . Mol Microbiol 67:, 241–253. [CrossRef][PubMed]
    [Google Scholar]
  62. Leday T. V., Gold K. M., Kinkel T. L., Roberts S. A., Scott J. R., McIver K. S.. ( 2008;). TrxR, a new CovR-repressed response regulator that activates the Mga virulence regulon in group A Streptococcus. . Infect Immun 76:, 4659–4668. [CrossRef][PubMed]
    [Google Scholar]
  63. Lenz D. H., Mok K. C., Lilley B. N., Kulkarni R. V., Wingreen N. S., Bassler B. L.. ( 2004;). The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. . Cell 118:, 69–82. [CrossRef][PubMed]
    [Google Scholar]
  64. Lilley B. N., Bassler B. L.. ( 2000;). Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. . Mol Microbiol 36:, 940–954. [CrossRef][PubMed]
    [Google Scholar]
  65. Lyon G. J., Novick R. P.. ( 2004;). Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. . Peptides 25:, 1389–1403. [CrossRef][PubMed]
    [Google Scholar]
  66. Lyristis M., Bryant A. E., Sloan J., Awad M. M., Nisbet I. T., Stevens D. L., Rood J. I.. ( 1994;). Identification and molecular analysis of a locus that regulates extracellular toxin production in Clostridium perfringens. . Mol Microbiol 12:, 761–777. [CrossRef][PubMed]
    [Google Scholar]
  67. Madhugiri R., Basineni S. R., Klug G.. ( 2010;). Turn-over of the small non-coding RNA RprA in E. coli is influenced by osmolarity. . Mol Genet Genomics 284:, 307–318. [CrossRef][PubMed]
    [Google Scholar]
  68. 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. [CrossRef][PubMed]
    [Google Scholar]
  69. Mandin P., Gottesman S.. ( 2010;). Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. . EMBO J 29:, 3094–3107. [CrossRef][PubMed]
    [Google Scholar]
  70. Mangold M., Siller M., Roppenser B., Vlaminckx B. J. M., Penfound T. A., Klein R., Novak R., Novick R. P., Charpentier E.. ( 2004;). Synthesis of group A streptococcal virulence factors is controlled by a regulatory RNA molecule. . Mol Microbiol 53:, 1515–1527. [CrossRef][PubMed]
    [Google Scholar]
  71. Massé 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. [CrossRef][PubMed]
    [Google Scholar]
  72. Massé E., Escorcia F. E., Gottesman S.. ( 2003;). Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. . Genes Dev 17:, 2374–2383. [CrossRef][PubMed]
    [Google Scholar]
  73. Massé E., Salvail H., Desnoyers G., Arguin M.. ( 2007;). Small RNAs controlling iron metabolism. . Curr Opin Microbiol 10:, 140–145. [CrossRef][PubMed]
    [Google Scholar]
  74. Mey A. R., Craig S. A., Payne S. M.. ( 2005;). Characterization of Vibrio cholerae RyhB: the RyhB regulon and role of ryhB in biofilm formation. . Infect Immun 73:, 5706–5719. [CrossRef][PubMed]
    [Google Scholar]
  75. Mika F., Hengge R.. ( 2013;). Small regulatory RNAs in the control of motility and biofilm formation in E. coli and Salmonella. . Int J Mol Sci 14:, 4560–4579. [CrossRef][PubMed]
    [Google Scholar]
  76. Miller M. B., Skorupski K., Lenz D. H., Taylor R. K., Bassler B. L.. ( 2002;). Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. . Cell 110:, 303–314. [CrossRef][PubMed]
    [Google Scholar]
  77. Modi S. R., Camacho D. M., Kohanski M. A., Walker G. C., Collins J. J.. ( 2011;). Functional characterization of bacterial sRNAs using a network biology approach. . Proc Natl Acad Sci U S A 108:, 15522–15527. [CrossRef][PubMed]
    [Google Scholar]
  78. Monteiro C., Papenfort K., Hentrich K., Ahmad I., Le Guyon S., Reimann R., Grantcharova N., Römling U.. ( 2012;). Hfq and Hfq-dependent small RNAs are major contributors to multicellular development in Salmonella enterica serovar Typhimurium. . RNA Biol 9:, 489–502. [CrossRef][PubMed]
    [Google Scholar]
  79. Moore S. D., Sauer R. T.. ( 2007;). The tmRNA system for translational surveillance and ribosome rescue. . Annu Rev Biochem 76:, 101–124. [CrossRef][PubMed]
    [Google Scholar]
  80. 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]
    [Google Scholar]
  81. Morita T., Kawamoto H., Mizota T., Inada T., Aiba H.. ( 2004;). Enolase in the RNA degradosome plays a crucial role in the rapid decay of glucose transporter mRNA in the response to phosphosugar stress in Escherichia coli. . Mol Microbiol 54:, 1063–1075. [CrossRef][PubMed]
    [Google Scholar]
  82. 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. [CrossRef][PubMed]
    [Google Scholar]
  83. Moulder J. W.. ( 1991;). Interaction of chlamydiae and host cells in vitro. . Microbiol Rev 55:, 143–190.[PubMed]
    [Google Scholar]
  84. Mraheil M. A., Billion A., Kuenne C., Pischimarov J., Kreikemeyer B., Engelmann S., Hartke A., Giard J.-C., Rupnik M.. & other authors ( 2010;). Comparative genome-wide analysis of small RNAs of major Gram-positive pathogens: from identification to application. . Microb Biotechnol 3:, 658–676. [CrossRef][PubMed]
    [Google Scholar]
  85. Mraheil M. A., Billion A., Mohamed W., Mukherjee K., Kuenne C., Pischimarov J., Krawitz C., Retey J., Hartsch T.. & other authors ( 2011;). The intracellular sRNA transcriptome of Listeria monocytogenes during growth in macrophages. . Nucleic Acids Res 39:, 4235–4248. [CrossRef][PubMed]
    [Google Scholar]
  86. Mulcahy H., O’Callaghan J., O’Grady E. P., Maciá M. D., Borrell N., Gómez C., Casey P. G., Hill C., Adams C.. & other authors ( 2008;). Pseudomonas aeruginosa RsmA plays an important role during murine infection by influencing colonization, virulence, persistence, and pulmonary inflammation. . Infect Immun 76:, 632–638. [CrossRef][PubMed]
    [Google Scholar]
  87. Novick R. P.. ( 2003;). Autoinduction and signal transduction in the regulation of staphylococcal virulence. . Mol Microbiol 48:, 1429–1449. [CrossRef][PubMed]
    [Google Scholar]
  88. Novick R. P., Geisinger E.. ( 2008;). Quorum sensing in staphylococci. . Annu Rev Genet 42:, 541–564. [CrossRef][PubMed]
    [Google Scholar]
  89. Novick R. P., Muir T. W.. ( 1999;). Virulence gene regulation by peptides in staphylococci and other Gram-positive bacteria. . Curr Opin Microbiol 2:, 40–45. [CrossRef][PubMed]
    [Google Scholar]
  90. Novick R. P., Ross H. F., Projan S. J., Kornblum J., Kreiswirth B., Moghazeh S.. ( 1993;). Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. . EMBO J 12:, 3967–3975.[PubMed]
    [Google Scholar]
  91. Obana N., Nomura N., Nakamura K.. ( 2013;). Structural requirement in Clostridium perfringens collagenase mRNA 5′ leader sequence for translational induction through small RNA-mRNA base pairing. . J Bacteriol 195:, 2937–2946. [CrossRef][PubMed]
    [Google Scholar]
  92. Ogawa W., Kim Y. M., Mizushima T., Tsuchiya T.. ( 1998;). Cloning and expression of the gene for the Na+-coupled serine transporter from Escherichia coli and characteristics of the transporter. . J Bacteriol 180:, 6749–6752.[PubMed]
    [Google Scholar]
  93. Ohtani K., Kawsar H. I., Okumura K., Hayashi H., Shimizu T.. ( 2003;). The VirR/VirS regulatory cascade affects transcription of plasmid-encoded putative virulence genes in Clostridium perfringens strain 13. . FEMS Microbiol Lett 222:, 137–141. [CrossRef][PubMed]
    [Google Scholar]
  94. Opdyke J. A., Kang J.-G., Storz G.. ( 2004;). GadY, a small-RNA regulator of acid response genes in Escherichia coli. . J Bacteriol 186:, 6698–6705. [CrossRef][PubMed]
    [Google Scholar]
  95. Opdyke J. A., Fozo E. M., Hemm M. R., Storz G.. ( 2011;). RNase III participates in GadY-dependent cleavage of the gadXgadW mRNA. . J Mol Biol 406:, 29–43. [CrossRef][PubMed]
    [Google Scholar]
  96. Papenfort K., Pfeiffer V., Mika F., Lucchini S., Hinton J. C. D., Vogel J.. ( 2006;). ΣE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. . Mol Microbiol 62:, 1674–1688. [CrossRef][PubMed]
    [Google Scholar]
  97. Papenfort K., Sun Y., Miyakoshi M., Vanderpool C. K., Vogel J.. ( 2013;). Small RNA-mediated activation of sugar phosphatase mRNA regulates glucose homeostasis. . Cell 153:, 426–437. [CrossRef][PubMed]
    [Google Scholar]
  98. Pellin D., Miotto P., Ambrosi A., Cirillo D. M., Di Serio C.. ( 2012;). A genome-wide identification analysis of small regulatory RNAs in Mycobacterium tuberculosis by RNA-Seq and conservation analysis. . PLoS ONE 7:, e32723. [CrossRef][PubMed]
    [Google Scholar]
  99. Petrova O. E., Sauer K.. ( 2010;). The novel two-component regulatory system BfiSR regulates biofilm development by controlling the small RNA rsmZ through CafA. . J Bacteriol 192:, 5275–5288. [CrossRef][PubMed]
    [Google Scholar]
  100. Pichon C., Felden B.. ( 2008;). Small RNA gene identification and mRNA target predictions in bacteria. . Bioinformatics 24:, 2807–2813. [CrossRef][PubMed]
    [Google Scholar]
  101. Podkaminski D., Vogel J.. ( 2010;). Small RNAs promote mRNA stability to activate the synthesis of virulence factors. . Mol Microbiol 78:, 1327–1331. [CrossRef][PubMed]
    [Google Scholar]
  102. Pulvermacher S. C., Stauffer L. T., Stauffer G. V.. ( 2009;). The small RNA GcvB regulates sstT mRNA expression in Escherichia coli. . J Bacteriol 191:, 238–248. [CrossRef][PubMed]
    [Google Scholar]
  103. Ramani N., Hedeshian M., Freundlich M.. ( 1994;). micF antisense RNA has a major role in osmoregulation of OmpF in Escherichia coli. . J Bacteriol 176:, 5005–5010.[PubMed]
    [Google Scholar]
  104. Revelles O., Millard P., Nougayrède J.-P., Dobrindt U., Oswald E., Létisse F., Portais J.-C.. ( 2013;). The carbon storage regulator (Csr) system exerts a nutrient-specific control over central metabolism in Escherichia coli strain Nissle 1917. . PLoS ONE 8:, e66386. [CrossRef][PubMed]
    [Google Scholar]
  105. Rice J. B., Vanderpool C. K.. ( 2011;). The small RNA SgrS controls sugar-phosphate accumulation by regulating multiple PTS genes. . Nucleic Acids Res 39:, 3806–3819. [CrossRef][PubMed]
    [Google Scholar]
  106. Richards G. R., Vanderpool C. K.. ( 2011;). Molecular call and response: the physiology of bacterial small RNAs. . Biochim Biophys Acta 1809:, 525–531. [CrossRef][PubMed]
    [Google Scholar]
  107. Richter C., Chang J. T., Fineran P. C.. ( 2012;). Function and regulation of clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR associated (Cas) systems. . Viruses 4:, 2291–2311. [CrossRef][PubMed]
    [Google Scholar]
  108. Roberts S. A., Scott J. R.. ( 2007;). RivR and the small RNA RivX: the missing links between the CovR regulatory cascade and the Mga regulon. . Mol Microbiol 66:, 1506–1522.[PubMed]
    [Google Scholar]
  109. Romeo T., Gong M., Liu M. Y., Brun-Zinkernagel A. M.. ( 1993;). Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. . J Bacteriol 175:, 4744–4755.[PubMed]
    [Google Scholar]
  110. Romeo T., Vakulskas C. A., Babitzke P.. ( 2013;). Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. . Environ Microbiol 15:, 313–324. [CrossRef][PubMed]
    [Google Scholar]
  111. Rutherford S. T., van Kessel J. C., Shao Y., Bassler B. L.. ( 2011;). AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. . Genes Dev 25:, 397–408. [CrossRef][PubMed]
    [Google Scholar]
  112. Salmon K., Hung S. P., Mekjian K., Baldi P., Hatfield G. W., Gunsalus R. P.. ( 2003;). Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. . J Biol Chem 278:, 29837–29855. [CrossRef][PubMed]
    [Google Scholar]
  113. Salvail H., Lanthier-Bourbonnais P., Sobota J. M., Caza M., Benjamin J.-A. M., Mendieta M. E. S., Lépine F., Dozois C. M., Imlay J., Massé E.. ( 2010;). A small RNA promotes siderophore production through transcriptional and metabolic remodeling. . Proc Natl Acad Sci U S A 107:, 15223–15228. [CrossRef][PubMed]
    [Google Scholar]
  114. Sharma C. M., Vogel J.. ( 2009;). Experimental approaches for the discovery and characterization of regulatory small RNA. . Curr Opin Microbiol 12:, 536–546. [CrossRef][PubMed]
    [Google Scholar]
  115. Sharma C. M., Darfeuille F., Plantinga T. H., 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. [CrossRef][PubMed]
    [Google Scholar]
  116. Sharma C. M., Papenfort K., Pernitzsch S. R., Mollenkopf H.-J., Hinton J. C. D., 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. [CrossRef][PubMed]
    [Google Scholar]
  117. Shaw E. I., Dooley C. A., Fischer E. R., Scidmore M. A., Fields K. A., Hackstadt T.. ( 2000;). Three temporal classes of gene expression during the Chlamydia trachomatis developmental cycle. . Mol Microbiol 37:, 913–925. [CrossRef][PubMed]
    [Google Scholar]
  118. Shenkman B., Varon D., Tamarin I., Dardik R., Peisachov M., Savion N., Rubinstein E.. ( 2002;). Role of agr (RNAIII) in Staphylococcus aureus adherence to fibrinogen, fibronectin, platelets and endothelial cells under static and flow conditions. . J Med Microbiol 51:, 747–754.[PubMed]
    [Google Scholar]
  119. Shimizu T., Yaguchi H., Ohtani K., Banu S., Hayashi H.. ( 2002;). Clostridial VirR/VirS regulon involves a regulatory RNA molecule for expression of toxins. . Mol Microbiol 43:, 257–265. [CrossRef][PubMed]
    [Google Scholar]
  120. Shioya K., Michaux C., Kuenne C., Hain T., Verneuil N., Budin-Verneuil A., Hartsch T., Hartke A., Giard J.-C.. ( 2011;). Genome-wide identification of small RNAs in the opportunistic pathogen Enterococcus faecalis V583. . PLoS ONE 6:, e23948. [CrossRef][PubMed]
    [Google Scholar]
  121. Silvaggi J. M., Perkins J. B., Losick R.. ( 2006;). Genes for small, noncoding RNAs under sporulation control in Bacillus subtilis. . J Bacteriol 188:, 532–541. [CrossRef][PubMed]
    [Google Scholar]
  122. Sorek R., Kunin V., Hugenholtz P.. ( 2008;). CRISPR – a widespread system that provides acquired resistance against phages in bacteria and archaea. . Nat Rev Microbiol 6:, 181–186. [CrossRef][PubMed]
    [Google Scholar]
  123. Sorger-Domenigg T., Sonnleitner E., Kaberdin V. R., Bläsi U.. ( 2007;). Distinct and overlapping binding sites of Pseudomonas aeruginosa Hfq and RsmA proteins on the non-coding RNA RsmY. . Biochem Biophys Res Commun 352:, 769–773. [CrossRef][PubMed]
    [Google Scholar]
  124. Steuten B., Schneider S., Wagner R.. ( 2014;). 6S RNA: recent answers – future questions. . Mol Microbiol 91:, 641–648. [CrossRef][PubMed]
    [Google Scholar]
  125. Storz G., Vogel J., Wassarman K. M.. ( 2011;). Regulation by small RNAs in bacteria: expanding frontiers. . Mol Cell 43:, 880–891. [CrossRef][PubMed]
    [Google Scholar]
  126. Svenningsen S. L., Tu K. C., Bassler B. L.. ( 2009;). Gene dosage compensation calibrates four regulatory RNAs to control Vibrio cholerae quorum sensing. . EMBO J 28:, 429–439. [CrossRef][PubMed]
    [Google Scholar]
  127. Thomason M. K., 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. [CrossRef][PubMed]
    [Google Scholar]
  128. Toledo-Arana A., Repoila F., Cossart P.. ( 2007;). Small noncoding RNAs controlling pathogenesis. . Curr Opin Microbiol 10:, 182–188. [CrossRef][PubMed]
    [Google Scholar]
  129. Tramonti A., Visca P., De Canio M., Falconi M., De Biase D.. ( 2002;). Functional characterization and regulation of gadX, a gene encoding an AraC/XylS-like transcriptional activator of the Escherichia coli glutamic acid decarboxylase system. . J Bacteriol 184:, 2603–2613. [CrossRef][PubMed]
    [Google Scholar]
  130. Trotochaud A. E., Wassarman K. M.. ( 2006;). 6S RNA regulation of pspF transcription leads to altered cell survival at high pH. . J Bacteriol 188:, 3936–3943. [CrossRef][PubMed]
    [Google Scholar]
  131. Urbanowski M. L., Stauffer L. T., Stauffer G. V.. ( 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. [CrossRef][PubMed]
    [Google Scholar]
  132. Vanderpool C. K., 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. [CrossRef][PubMed]
    [Google Scholar]
  133. Vecerek B., Moll I., Bläsi U.. ( 2007;). Control of Fur synthesis by the non-coding RNA RyhB and iron-responsive decoding. . EMBO J 26:, 965–975. [CrossRef][PubMed]
    [Google Scholar]
  134. Vogel J.. ( 2009;). A rough guide to the non-coding RNA world of Salmonella. . Mol Microbiol 71:, 1–11. [CrossRef][PubMed]
    [Google Scholar]
  135. Vogel J., Sharma C. M.. ( 2005;). How to find small non-coding RNAs in bacteria. . Biol Chem 386:, 1219–1238. [CrossRef][PubMed]
    [Google Scholar]
  136. Vogel J., Wagner E. G. H.. ( 2007;). Target identification of small noncoding RNAs in bacteria. . Curr Opin Microbiol 10:, 262–270. [CrossRef][PubMed]
    [Google Scholar]
  137. Wassarman K. M.. ( 2007;). 6S RNA: a small RNA regulator of transcription. . Curr Opin Microbiol 10:, 164–168. [CrossRef][PubMed]
    [Google Scholar]
  138. Wassarman K. M., Repoila F., Rosenow C., Storz G., Gottesman S.. ( 2001;). Identification of novel small RNAs using comparative genomics and microarrays. . Genes Dev 15:, 1637–1651. [CrossRef][PubMed]
    [Google Scholar]
  139. Waters C. M., Bassler B. L.. ( 2005;). Quorum sensing: cell-to-cell communication in bacteria. . Annu Rev Cell Dev Biol 21:, 319–346. [CrossRef][PubMed]
    [Google Scholar]
  140. Waters L. S., Storz G.. ( 2009;). Regulatory RNAs in bacteria. . Cell 136:, 615–628. [CrossRef][PubMed]
    [Google Scholar]
  141. Weaver K. E.. ( 2012;). The par toxin–antitoxin system from Enterococcus faecalis plasmid pAD1 and its chromosomal homologs. . RNA Biol 9:, 1498–1503. [CrossRef][PubMed]
    [Google Scholar]
  142. Wilderman P. J., Sowa N. A., FitzGerald D. J., FitzGerald P. C., Gottesman S., Ochsner U. A., Vasil M. L.. ( 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. [CrossRef][PubMed]
    [Google Scholar]
  143. Winkler W. C., Breaker R. R.. ( 2005;). Regulation of bacterial gene expression by riboswitches. . Annu Rev Microbiol 59:, 487–517. [CrossRef][PubMed]
    [Google Scholar]
  144. 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. [CrossRef][PubMed]
    [Google Scholar]
  145. Zhang A., Wassarman K. M., Rosenow C., Tjaden B. C., Storz G., Gottesman S.. ( 2003;). Global analysis of small RNA and mRNA targets of Hfq. . Mol Microbiol 50:, 1111–1124. [CrossRef][PubMed]
    [Google Scholar]
  146. Zhang Y., Zhang Z., Ling L., Shi B., Chen R.. ( 2004;). Conservation analysis of small RNA genes in Escherichia coli. . Bioinformatics 20:, 599–603. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.076208-0
Loading
/content/journal/micro/10.1099/mic.0.076208-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error