1932

Abstract

Noncoding RNAs (ncRNAs) regulating virulence have been identified in most pathogens. This review discusses RNA-mediated mechanisms exploited by bacterial pathogens to successfully infect and colonize their hosts. It discusses the most representative RNA-mediated regulatory mechanisms employed by two intracellular [ and serovar Typhimurium (. Typhimurium)] and two extracellular ( and ) bacterial pathogens. We review the RNA-mediated regulators (e.g., thermosensors, riboswitches, - and -encoded RNAs) used for adaptation to the specific niches colonized by these bacteria (intestine, blood, or the intracellular environment, for example) in the framework of the specific pathophysiological aspects of the diseases caused by these microorganisms. A critical discussion of the newest findings in the field of bacterial ncRNAs shows how examples in model pathogens could pave the way for the discovery of new mechanisms in other medically important bacterial pathogens.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-030117-020335
2017-09-08
2024-06-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/71/1/annurev-micro-030117-020335.html?itemId=/content/journals/10.1146/annurev-micro-030117-020335&mimeType=html&fmt=ahah

Literature Cited

  1. Albrecht M, Sharma CM, Reinhardt R, Vogel J, Rudel T. 1.  2010. Deep sequencing-based discovery of the Chlamydia trachomatis transcriptome. Nucleic Acids Res 38:868–77 [Google Scholar]
  2. Almagro-Moreno S, Pruss K, Taylor RK. 2.  2015. Intestinal colonization dynamics of Vibrio cholerae. PLOS Pathog. 11:e1004787 [Google Scholar]
  3. Archambaud C, Nahori MA, Soubigou G, Becavin C, Laval L. 3.  et al. 2012. Impact of lactobacilli on orally acquired listeriosis. PNAS 109:16684–89 [Google Scholar]
  4. Archambaud C, Sismeiro O, Toedling J, Soubigou G, Becavin C. 4.  et al. 2013. The intestinal microbiota interferes with the microRNA response upon oral Listeria infection. mBio 4:e00707–13 [Google Scholar]
  5. Arciola CR, Campoccia D, Speziale P, Montanaro L, Costerton JW. 5.  2012. Biofilm formation in Staphylococcus implant infections: a review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials 33:5967–82 [Google Scholar]
  6. Bandyra KJ, Said N, Pfeiffer V, Gorna MW, Vogel J, Luisi BF. 6.  2012. The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol. Cell 47:943–53 [Google Scholar]
  7. Barquist L, Vogel J. 7.  2015. Accelerating discovery and functional analysis of small RNAs with new technologies. Annu. Rev. Genet. 49:367–94 [Google Scholar]
  8. Blenkiron C, Simonov D, Muthukaruppan A, Tsai P, Dauros P. 8.  et al. 2016. Uropathogenic Escherichia coli releases extracellular vesicles that are associated with RNA. PLOS ONE 11:e0160440 [Google Scholar]
  9. Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N. 9.  et al. 2007. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21:1353–66 [Google Scholar]
  10. Bossi L, Schwartz A, Guillemardet B, Boudvillain M, Figueroa-Bossi N. 10.  2012. A role for Rho-dependent polarity in gene regulation by a noncoding small RNA. Genes Dev 26:1864–73 [Google Scholar]
  11. Bronesky D, Wu Z, Marzi S, Walter P, Geissmann T. 11.  et al. 2016. Staphylococcus aureus RNAIII and its regulon link quorum sensing, stress responses, metabolic adaptation, and regulation of virulence gene expression. Annu. Rev. Microbiol. 70:299–316 [Google Scholar]
  12. Buchrieser C, Rusniok C. Kunst F, Cossart P, Glaser P. 12. , The Listeria Consortium, 2003. Comparison of the genome sequences of Listeria monocytogenes and Listeria innocua: clues for evolution and pathogenicity. FEMS Immunol. Med. Microbiol 35:207–13 [Google Scholar]
  13. Burnett JC, Rossi JJ. 13.  2012. RNA-based therapeutics: current progress and future prospects. Chem. Biol. 19:60–71 [Google Scholar]
  14. Caldelari I, Chao Y, Romby P, Vogel J. 14.  2013. RNA-mediated regulation in pathogenic bacteria. Cold Spring Harb. Perspect. Med. 3:a010298 [Google Scholar]
  15. Chabelskaya S, Bordeau V, Felden B. 15.  2014. Dual RNA regulatory control of a Staphylococcus aureus virulence factor. Nucleic Acids Res 42:4847–58 [Google Scholar]
  16. Chao Y, Papenfort K, Reinhardt R, Sharma CM, Vogel J. 16.  2012. An atlas of Hfq-bound transcripts reveals 3′ UTRs as a genomic reservoir of regulatory small RNAs. EMBO J 31:4005–19 [Google Scholar]
  17. Chao Y, Vogel J. 17.  2016. A 3′ UTR-derived small RNA provides the regulatory noncoding arm of the inner membrane stress response. Mol. Cell 61:352–63 [Google Scholar]
  18. Charpentier E, Richter H, van der Oost J, White MF. 18.  2015. Biogenesis pathways of RNA guides in archaeal and bacterial CRISPR-Cas adaptive immunity. FEMS Microbiol. Rev. 39:428–41 [Google Scholar]
  19. Chevalier C, Boisset S, Romilly C, Masquida B, Fechter P. 19.  et al. 2010. Staphylococcus aureus RNAIII binds to two distant regions of coa mRNA to arrest translation and promote mRNA degradation. PLOS Pathog 6:e1000809 [Google Scholar]
  20. Cossart P. 20.  2011. Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. PNAS 108:19484–91 [Google Scholar]
  21. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F. 21.  1999. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun 67:5427–33 [Google Scholar]
  22. Dar D, Shamir M, Mellin JR, Koutero M, Stern-Ginossar N. 22.  et al. 2016. Term-seq reveals abundant ribo-regulation of antibiotics resistance in bacteria. Science 352:aad9822 [Google Scholar]
  23. Davies BW, Bogard RW, Young TS, Mekalanos JJ. 23.  2012. Coordinated regulation of accessory genetic elements produces cyclic di-nucleotides for V.cholerae virulence. Cell 149:358–70 [Google Scholar]
  24. DebRoy S, Gebbie M, Ramesh A, Goodson JR, Cruz MR. 24.  et al. 2014. A riboswitch-containing sRNA controls gene expression by sequestration of a response regulator. Science 345:937–40 [Google Scholar]
  25. Duval M, Cossart P, Lebreton A. 25.  2017. Mammalian microRNAs and long noncoding RNAs in the host-bacterial pathogen crosstalk. Semin. Cell Dev. Biol. 65:11–19 [Google Scholar]
  26. Fei J, Singh D, Zhang Q, Park S, Balasubramanian D. 26.  et al. 2015. RNA biochemistry: determination of in vivo target search kinetics of regulatory noncoding RNA. Science 347:1371–74 [Google Scholar]
  27. Frohlich KS, Papenfort K, Fekete A, Vogel J. 27.  2013. A small RNA activates CFA synthase by isoform-specific mRNA stabilization. EMBO J 32:2963–79 [Google Scholar]
  28. Frohlich KS, Vogel J. 28.  2009. Activation of gene expression by small RNA. Curr. Opin. Microbiol. 12:674–82 [Google Scholar]
  29. Galan JE. 29.  2001. Salmonella interactions with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17:53–86 [Google Scholar]
  30. Garzoni C, Kelley WL. 30.  2009. Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol 17:59–65 [Google Scholar]
  31. Geisinger E, Adhikari RP, Jin R, Ross HF, Novick RP. 31.  2006. Inhibition of rot translation by RNAIII, a key feature of agr function. Mol. Microbiol 61:1038–48 [Google Scholar]
  32. Gong H, Vu GP, Bai Y, Chan E, Wu R. 32.  et al. 2011. A Salmonella small non-coding RNA facilitates bacterial invasion and intracellular replication by modulating the expression of virulence factors. PLOS Pathog 7:e1002120 [Google Scholar]
  33. Gottesman S, Storz G. 33.  2011. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb. Perspect. Biol. 3:a003798 [Google Scholar]
  34. Hammer BK, Bassler BL. 34.  2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50:101–4 [Google Scholar]
  35. Harris JB, LaRocque RC, Qadri F, Ryan ET, Calderwood SB. 35.  2012. Cholera. Lancet 379:2466–76 [Google Scholar]
  36. Howden BP, Beaume M, Harrison PF, Hernandez D, Schrenzel J. 36.  et al. 2013. Analysis of the small RNA transcriptional response in multidrug-resistant Staphylococcus aureus after antimicrobial exposure. Antimicrob. Agents Chemother. 57:3864–74 [Google Scholar]
  37. Huntzinger E, Boisset S, Saveanu C, Benito Y, Geissmann T. 37.  et al. 2005. Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J 24:824–35 [Google Scholar]
  38. Janzon L, Arvidson S. 38.  1990. The role of the δ-lysin gene (hld) in the regulation of virulence genes by the accessory gene regulator (agr) in Staphylococcus aureus. EMBO J 9:1391–99 [Google Scholar]
  39. Jefferson KK, Cramton SE, Gotz F, Pier GB. 39.  2003. Identification of a 5-nucleotide sequence that controls expression of the ica locus in Staphylococcus aureus and characterization of the DNA-binding properties of IcaR. Mol. Microbiol 48:889–99 [Google Scholar]
  40. Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M, Cossart P. 40.  2002. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110:551–61 [Google Scholar]
  41. Kawamoto H, Koide Y, Morita T, Aiba H. 41.  2006. Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol. Microbiol. 61:1013–22 [Google Scholar]
  42. Kawano M, Reynolds AA, Miranda-Rios J, Storz G. 42.  2005. Detection of 5′- and 3′-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli. Nucleic Acids Res. 33:1040–50 [Google Scholar]
  43. Kim T, Bak G, Lee J, Kim KS. 43.  2015. Systematic analysis of the role of bacterial Hfq-interacting sRNAs in the response to antibiotics. J. Antimicrob. Chemother. 70:1659–68 [Google Scholar]
  44. LaRock DL, Chaudhary A, Miller SI. 44.  2015. Salmonellae interactions with host processes. Nat. Rev. Microbiol. 13:191–205 [Google Scholar]
  45. Lasa I, Toledo-Arana A, Dobin A, Villanueva M, de los Mozos IR. 45.  et al. 2011. Genome-wide antisense transcription drives mRNA processing in bacteria. PNAS 108:20172–77 [Google Scholar]
  46. Lebreton A, Cossart P. 46.  2017. RNA- and protein-mediated control of Listeria monocytogenes virulence gene expression. RNA Biol 14:460–70 [Google Scholar]
  47. Lee EJ, Choi J, Groisman EA. 47.  2014. Control of a Salmonella virulence operon by proline-charged tRNAPro. PNAS 111:3140–45 [Google Scholar]
  48. Lee EJ, Groisman EA. 48.  2012. Control of a Salmonella virulence locus by an ATP-sensing leader messenger RNA. Nature 486:271–75 [Google Scholar]
  49. Lee EJ, Groisman EA. 49.  2012. Tandem attenuators control expression of the Salmonella mgtCBR virulence operon. Mol. Microbiol. 86:212–24 [Google Scholar]
  50. Lee EJ, Pontes MH, Groisman EA. 50.  2013. A bacterial virulence protein promotes pathogenicity by inhibiting the bacterium's own F1Fo ATP synthase. Cell 154:146–56 [Google Scholar]
  51. Lee JW, Lee EJ. 51.  2015. Regulation and function of the Salmonella MgtC virulence protein. J. Microbiol. 53:667–72 [Google Scholar]
  52. Lee SW, Mitchell DA, Markley AL, Hensler ME, Gonzalez D. 52.  et al. 2008. Discovery of a widely distributed toxin biosynthetic gene cluster. PNAS 105:5879–84 [Google Scholar]
  53. Liu H, Wang X, Wang HD, Wu J, Ren J. 53.  et al. 2012. Escherichiacoli noncoding RNAs can affect gene expression and physiology of Caenorhabditis elegans. Nat. Commun. 3:1073 [Google Scholar]
  54. Liu S, da Cunha AP, Rezende RM, Cialic R, Wei Z. 54.  et al. 2016. The host shapes the gut microbiota via fecal microRNA. Cell Host Microbe 19:32–43 [Google Scholar]
  55. Loh E, Dussurget O, Gripenland J, Vaitkevicius K, Tiensuu T. 55.  et al. 2009. A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 139:770–79 [Google Scholar]
  56. Lopez-Montero N, Ramos-Marques E, Risco C, Garcia-del Portillo F. 56.  2016. Intracellular Salmonella induces aggrephagy of host endomembranes in persistent infections. Autophagy 12:1886–1901 [Google Scholar]
  57. Lowden MJ, Skorupski K, Pellegrini M, Chiorazzo MG, Taylor RK, Kull FJ. 57.  2010. Structure of Vibrio cholerae ToxT reveals a mechanism for fatty acid regulation of virulence genes. PNAS 107:2860–65 [Google Scholar]
  58. Lundin KE, Gissberg O, Smith CI. 58.  2015. Oligonucleotide therapies: the past and the present. Hum. Gene Ther. 26:475–85 [Google Scholar]
  59. Mandlik A, Livny J, Robins WP, Ritchie JM, Mekalanos JJ, Waldor MK. 59.  2011. RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. Cell Host Microbe 10:165–74 [Google Scholar]
  60. Mellin JR, Cossart P. 60.  2015. Unexpected versatility in bacterial riboswitches. Trends Genet 31:150–56 [Google Scholar]
  61. Mellin JR, Koutero M, Dar D, Nahori MA, Sorek R, Cossart P. 61.  2014. Sequestration of a two-component response regulator by a riboswitch-regulated noncoding RNA. Science 345:940–43 [Google Scholar]
  62. Mellin JR, Tiensuu T, Becavin C, Gouin E, Johansson J, Cossart P. 62.  2013. A riboswitch-regulated antisense RNA in Listeria monocytogenes. PNAS 110:13132–37 [Google Scholar]
  63. Morfeldt E, Taylor D, von Gabain A, Arvidson S. 63.  1995. Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J 14:4569–77 [Google Scholar]
  64. Nechooshtan G, Elgrably-Weiss M, Altuvia S. 64.  2014. Changes in transcriptional pausing modify the folding dynamics of the pH-responsive RNA element. Nucleic Acids Res 42:622–30 [Google Scholar]
  65. Novick RP, Geisinger E. 65.  2008. Quorum sensing in staphylococci. Annu. Rev. Genet. 42:541–64 [Google Scholar]
  66. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, Moghazeh S. 66.  1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12:3967–75 [Google Scholar]
  67. Oliva G, Sahr T, Buchrieser C. 67.  2015. Small RNAs, 5′ UTR elements and RNA-binding proteins in intracellular bacteria: impact on metabolism and virulence. FEMS Microbiol. Rev. 39:331–49 [Google Scholar]
  68. Ortega AD, Quereda JJ, Pucciarelli MG, Garcia-del Portillo F. 68.  2014. Non-coding RNA regulation in pathogenic bacteria located inside eukaryotic cells. Front. Cell Infect. Microbiol. 4:162 [Google Scholar]
  69. Papenfort K, Forstner KU, Cong JP, Sharma CM, Bassler BL. 69.  2015. Differential RNA-seq of Vibrio cholerae identifies the VqmR small RNA as a regulator of biofilm formation. PNAS 112:E766–75 [Google Scholar]
  70. Pinel-Marie ML, Brielle R, Felden B. 70.  2014. Dual toxic-peptide-coding Staphylococcus aureus RNA under antisense regulation targets host cells and bacterial rivals unequally. Cell Rep 7:424–35 [Google Scholar]
  71. Pizarro-Cerda J, Kuhbacher A, Cossart P. 71.  2012. Entry of Listeria monocytogenes in mammalian epithelial cells: an updated view. Cold Spring Harb. Perspect. Med. 2:a010009 [Google Scholar]
  72. Quereda JJ, Dussurget O, Nahori MA, Ghozlane A, Volant S. 72.  et al. 2016. Bacteriocin from epidemic Listeria strains alters the host intestinal microbiota to favor infection. PNAS 113:5706–11 [Google Scholar]
  73. Quereda JJ, Garcia-Del Portillo F, Pucciarelli MG. 73.  2016. Listeria monocytogenes remodels the cell surface in the blood-stage. Environ. Microbiol. Rep. 8:641–48 [Google Scholar]
  74. Quereda JJ, Ortega AD, Pucciarelli MG, Garcia-Del Portillo F. 74.  2014. The Listeria small RNA Rli27 regulates a cell wall protein inside eukaryotic cells by targeting a long 5′-UTR variant. PLOS Genet 10:e1004765 [Google Scholar]
  75. Quereda JJ, Pizarro-Cerda J, Balestrino D, Bobard A, Danckaert A. 75.  et al. 2015. A dual microscopy-based assay to assess Listeria monocytogenes cellular entry and vacuolar escape. Appl. Environ. Microbiol. 82:211–17 [Google Scholar]
  76. Quereda JJ, Pucciarelli MG. 76.  2014. Deletion of the membrane protein Lmo0412 increases the virulence of Listeria monocytogenes. Microbes Infect. 16:623–32 [Google Scholar]
  77. Ribet D, Cossart P. 77.  2015. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect 17:173–83 [Google Scholar]
  78. Ruiz de los Mozos I, Vergara-Irigaray M, Segura V, Villanueva M, Bitarte N. 78.  et al. 2013. Base pairing interaction between 5′- and 3′-UTRs controls icaR mRNA translation in Staphylococcus aureus. PLOS Genet 9:e1004001 [Google Scholar]
  79. Rutherford ST, van Kessel JC, Shao Y, Bassler BL. 79.  2011. AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev 25:397–408 [Google Scholar]
  80. Saliba AE, Westermann AJ, Gorski SA, Vogel J. 80.  2014. Single-cell RNA-seq: advances and future challenges. Nucleic Acids Res 42:8845–60 [Google Scholar]
  81. Sayed N, Jousselin A, Felden B. 81.  2012. A cis-antisense RNA acts in trans in Staphylococcus aureus to control translation of a human cytolytic peptide. Nat. Struct. Mol. Biol 19:105–12 [Google Scholar]
  82. Sayed N, Nonin-Lecomte S, Rety S, Felden B. 82.  2012. Functional and structural insights of a Staphylococcus aureus apoptotic-like membrane peptide from a toxin-antitoxin module. J. Biol. Chem. 287:43454–63 [Google Scholar]
  83. Sedlyarova N, Shamovsky I, Bharati BK, Epshtein V, Chen J. 83.  et al. 2016. sRNA-mediated control of transcription termination in E. coli. Cell 167:111–21.e13 [Google Scholar]
  84. Sesto N, Touchon M, Andrade JM, Kondo J, Rocha EP. 84.  et al. 2014. A PNPase dependent CRISPR system in Listeria. PLOS Genet. 10:e1004065 [Google Scholar]
  85. Sesto N, Wurtzel O, Archambaud C, Sorek R, Cossart P. 85.  2013. The excludon: a new concept in bacterial antisense RNA-mediated gene regulation. Nat. Rev. Microbiol. 11:75–82 [Google Scholar]
  86. Shao Y, Bassler BL. 86.  2012. Quorum-sensing non-coding small RNAs use unique pairing regions to differentially control mRNA targets. Mol. Microbiol. 83:599–611 [Google Scholar]
  87. Shao Y, Bassler BL. 87.  2014. Quorum regulatory small RNAs repress type VI secretion in Vibrio cholerae. Mol. Microbiol. 92:921–30 [Google Scholar]
  88. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S. 88.  et al. 2010. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464:250–55 [Google Scholar]
  89. Silva AJ, Benitez JA. 89.  2016. Vibrio cholerae biofilms and cholera pathogenesis. PLOS Negl. Trop. Dis. 10:e0004330 [Google Scholar]
  90. Skorupski K, Taylor RK. 90.  1999. A new level in the Vibrio cholerae ToxR virulence cascade: AphA is required for transcriptional activation of the tcpPH operon. Mol. Microbiol 31:763–71 [Google Scholar]
  91. Smirnov A, Forstner KU, Holmqvist E, Otto A, Gunster R. 91.  et al. 2016. Grad-seq guides the discovery of ProQ as a major small RNA-binding protein. PNAS 113:11591–96 [Google Scholar]
  92. Sonnleitner E, Gonzalez N, Sorger-Domenigg T, Heeb S, Richter AS. 92.  et al. 2011. The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal. Mol. Microbiol. 80:868–85 [Google Scholar]
  93. Srivastava D, Harris RC, Waters CM. 93.  2011. Integration of cyclic di-GMP and quorum sensing in the control of vpsT and aphA in Vibrio cholerae. J. Bacteriol 193:6331–41 [Google Scholar]
  94. Storz G, Vogel J, Wassarman KM. 94.  2011. Regulation by small RNAs in bacteria: expanding frontiers. Mol. Cell 43:880–91 [Google Scholar]
  95. Svensson SL, Sharma CM. 95.  2016. Small RNAs in bacterial virulence and communication. Microbiol. Spectr. 4:VMBF–0028-2015 [Google Scholar]
  96. Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V. 96.  et al. 2011. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. PNAS 108:17480–85 [Google Scholar]
  97. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H. 97.  et al. 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950–56 [Google Scholar]
  98. Traber KE, Lee E, Benson S, Corrigan R, Cantera M. 98.  et al. 2008. agr function in clinical Staphylococcus aureus isolates. Microbiology 154:2265–74 [Google Scholar]
  99. Wagner EGH, Romby P. 99.  2015. Small RNAs in bacteria and archaea: who they are, what they do, and how they do it. Adv. Genet. 90:133–208 [Google Scholar]
  100. Wassarman KM. 100.  2007. 6S RNA: a regulator of transcription. Mol. Microbiol. 65:1425–31 [Google Scholar]
  101. Waters CM, Lu W, Rabinowitz JD, Bassler BL. 101.  2008. Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J. Bacteriol. 190:2527–36 [Google Scholar]
  102. Waters LS, Storz G. 102.  2009. Regulatory RNAs in bacteria. Cell 136:615–28 [Google Scholar]
  103. Weber GG, Kortmann J, Narberhaus F, Klose KE. 103.  2014. RNA thermometer controls temperature-dependent virulence factor expression in Vibrio cholerae. PNAS 111:14241–46 [Google Scholar]
  104. Westermann AJ, Forstner KU, Amman F, Barquist L, Chao Y. 104.  et al. 2016. Dual RNA-seq unveils noncoding RNA functions in host-pathogen interactions. Nature 529:496–501 [Google Scholar]
  105. Westermann AJ, Gorski SA, Vogel J. 105.  2012. Dual RNA-seq of pathogen and host. Nat. Rev. Microbiol. 10:618–30 [Google Scholar]
  106. Wright AV, Nunez JK, Doudna JA. 106.  2016. Biology and applications of CRISPR systems: harnessing nature's toolbox for genome engineering. Cell 164:29–44 [Google Scholar]
  107. Wurtzel O, Yoder-Himes DR, Han K, Dandekar AA, Edelheit S. 107.  et al. 2012. The single-nucleotide resolution transcriptome of Pseudomonas aeruginosa grown in body temperature. PLOS Pathog 8:e1002945 [Google Scholar]
  108. Yu J, Schneiders T. 108.  2012. Tigecycline challenge triggers sRNA production in Salmonella enterica serovar Typhimurium. BMC Microbiol 12:195 [Google Scholar]
  109. Zheng J, Shin OS, Cameron DE, Mekalanos JJ. 109.  2010. Quorum sensing and a global regulator TsrA control expression of type VI secretion and virulence in Vibrio cholerae. PNAS 107:21128–33 [Google Scholar]
  110. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ. 110.  2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. PNAS 99:3129–34 [Google Scholar]
/content/journals/10.1146/annurev-micro-030117-020335
Loading
/content/journals/10.1146/annurev-micro-030117-020335
Loading

Data & Media loading...

  • Article Type: Review Article
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