Identification of novel sRNAs involved in biofilm formation, motility, and fimbriae formation in Escherichia coli

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Bak, Geunu ^a   Lee, Jungmin ^a   Suk, Shinae ^a   Kim, Daun ^a   Lee, Ji Young ^a   Kim, Kwang Sun ^b   Choi, Byong Seok ^a   Lee, Younghoon ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFILM; ESCHERICHIA COLI; FIMBRIA; GENE OVEREXPRESSION; METABOLISM; PHENOTYPE; PLASMID; TRANSCRIPTION REGULATION; GENE EXPRESSION REGULATION; GENETICS; NORTHERN BLOTTING; PHYSIOLOGY;

BACTERIAL RNA; ESCHERICHIA COLI PROTEIN;

BIOFILMS; BLOTTING, NORTHERN; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; PHENOTYPE; PLASMIDS; RNA, BACTERIAL;

EID: 84944340025     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep15287     Document Type: Article

References (73)

1. Rivas, E., Klein, R. J., Jones, T. A. & Eddy, S. R. Computational identification of noncoding RNAs in E. coli by comparative genomics. Curr Biol. 11, 1369-1373 (2001).
2. Argaman, L. et al. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol. 11, 941-950 (2001).
3. Chen, S. et al. A bioinformatics based approach to discover small RNA genes in the Escherichia coli genome. Biosystems. 65, 157-177 (2002).
4. Vogel, J. et al. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res. 31, 6435-6443 (2003).
5. Zhang, A. et al. Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol. 50, 1111-1124 (2003).
6. Wassarman, K. M., Repoila, F., Rosenow, C., Storz, G. & Gottesman, S. Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev. 15, 1637-1651 (2001).
7. Raghavan, R., Groisman, E. A. & Ochman, H. Genome-wide detection of novel regulatory RNAs in E. coli. Genome Res. 21, 1487-1497 (2011).
8. Tjaden, B. et al. Transcriptome analysis of Escherichia coli using high-density oligonucleotide probe arrays. Nucleic Acids Res. 30, 3732-3738 (2002).
9. Waters, L. S. & Storz, G. Regulatory RNAs in bacteria. Cell. 136, 615-628 (2009).
10. Gottesman, S. & Storz, G. Bacterial Small RNA Regulators: Versatile Roles and Rapidly Evolving Variations. Cold Spring Harb Perspect Biol. 3, a003987 (2010).
11. Storz, G., Vogel, J. & Wassarman, K. M. Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell. 43, 880-91 (2011).
12. Sharma, C. & Heidrich, N. Small RNAs and virulence in bacterial pathogens. RNA Biol. 9, 361-363 (2012).
13. Toledo-Arana, A., Repoila, F. & Cossart, P. Small noncoding RNAs controlling pathogenesis. Curr Opin Microbiol. 10, 182-188 (2007).
14. Papenfort, K. & Vogel, J. Regulatory RNA in bacterial pathogens. Cell Host Microbe. 8, 116-127 (2010).
15. Hoe, C.-H., Raabe, C. a, Rozhdestvensky, T. S. & Tang, T.-H. Bacterial sRNAs: regulation in stress. Int J Med Microbiol. 303, 217-29 (2013).
16. Vogel, J. & Luisi, B. F. Hfq and its constellation of RNA. Nat Rev Microbiol. 9, 578-89 (2011).
17. De Lay, N., Schu, D. J. & Gottesman, S. Bacterial small RNA-based negative regulation: Hfq and its accomplices. J Biol Chem. 288, 7996-8003 (2013).
18. Sobrero, P. & Valverde, C. The bacterial protein Hfq: much more than a mere RNA-binding factor. Crit Rev Microbiol. 38, 276-99 (2012).
19. Hall-Stoodley, L., Costerton, J. W. & Stoodley, P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2, 95-108 (2004).
20. Karatan, E. & Watnick, P. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev. 73, 310-47 (2009).
21. Lenz, A. P., Williamson, K. S., Pitts, B., Stewart, P. S. & Franklin, M. J. Localized gene expression in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol. 74, 4463-71 (2008).
22. Beloin, C. et al. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol. 51, 659-674 (2004).
23. Ren, D., Bedzyk, L. A., Thomas, S. M., Ye, R. W. & Wood, T. K. Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol. 64, 515-524 (2004).
24. Schembri, M. A., Kjaergaard, K. & Klemm, P. Global gene expression in Escherichia coli biofilms. Mol Microbiol. 48, 253-267 (2003).
25. Niba, E. T., Naka, Y., Nagase, M., Mori, H. & Kitakawa, M. A genome-wide approach to identify the genes involved in biofilm formation in E. coli. DNA Res. 14, 237-246 (2007).
26. Van Houdt, R. & Michiels, C. W. Role of bacterial cell surface structures in Escherichia coli biofilm formation. Res Microbiol. 156, 626-633 (2005).
27. Michaux, C., Verneuil, N., Hartke, A. & Giard, J.-C. Physiological roles of small RNA molecules. Microbiology. 160, 1007-19 (2014).
28. Guillier, M., Gottesman, S. & Storz, G. Modulating the outer membrane with small RNAs. Genes Dev. 20, 2338-2348 (2006).
29. Papenfort, K. & Vogel, J. Multiple target regulation by small noncoding RNAs rewires gene expression at the post-transcriptional level. Res Microbiol. 160, 278-287 (2009).
30. Mandin, P. & Gottesman, S. Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J. 29, 3094-3107 (2010).
31. De Lay, N. & Gottesman, S. A complex network of small non-coding RNAs regulate motility in Escherichia coli. Mol Microbiol. 86, 524-538 (2012).
32. Mika, F. & Hengge, R. Small Regulatory RNAs in the Control of Motility and Biofilm Formation in E. coli and Salmonella. Int J Mol Sci. 14, 4560-79 (2013).
33. Holmqvist, E. et al. Two antisense RNAs target the transcriptional regulator CsgD to inhibit curli synthesis. EMBO J. 29, 1840-1850 (2010).
34. Urban, J. H. & Vogel, J. Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol. 6, e64 (2008).
35. Lease, R. A. & Belfort, M. Riboregulation by DsrA RNA: trans-actions for global economy. Mol Microbiol. 38, 667-672 (2000).
36. Frohlich, K. S., Papenfort, K., Berger, A. A. & Vogel, J. A conserved RpoS-dependent small RNA controls the synthesis of major porin OmpD. Nucleic Acids Res. 40, 3623-3640 (2012).
37. Park, H., Bak, G., Kim, S. C. & Lee, Y. Exploring sRNA-mediated gene silencing mechanisms using artificial small RNAs derived from a natural RNA scaffold in Escherichia coli. Nucleic Acids Res. 41, 3787-3804 (2013).
38. Pratt, L. A. & Kolter, R. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol. 30, 285-293 (1998).
39. Verstraeten, N. et al. Living on a surface: swarming and biofilm formation. Trends Microbiol. 16, 496-506 (2008).
40. Harshey, R. M. Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol. 57, 249-273 (2003).
41. Vanderpool, C. K. & Gottesman, S. Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol. 54, 1076-1089 (2004).
42. Udekwu, K. I. et al. Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev. 19, 2355-2366 (2005).
43. Rasmussen, A. A. et al. Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase-dependent control. Mol Microbiol. 58, 1421-1429 (2005).
44. Romling, U. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci. 62, 1234-1246 (2005).
45. Prigent-Combaret, C. et al. Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol. 2, 450-64 (2000).
46. Schilling, J. D., Mulvey, M. A. & Hultgren, S. J. Structure and Function of Escherichia coli Type 1 Pili : New Insight into the Pathogenesis of Urinary Tract Infections. J Infect Dis. 183, S36-S40 (2001).
47. Hasman, H., Schembri, M. a. & Klemm, P. Antigen 43 and Type 1 Fimbriae Determine Colony Morphology of Escherichia coli K-12. J Bacteriol. 182, 1089-1095 (2000).
48. Johansen, J., Rasmussen, A. A., Overgaard, M. & Valentin-Hansen, P. Conserved small non-coding RNAs that belong to the sigmaE regulon: role in down-regulation of outer membrane proteins. J Mol Biol. 364, 1-8 (2006).
49. Gogol, E. B., Rhodius, V. a, Papenfort, K., Vogel, J. & Gross, C. A. Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon. Proc Natl Acad Sci USA 108, 12875-80 (2011).
50. Jorgensen, M. G. et al. Small regulatory RNAs control the multi-cellular adhesive lifestyle of Escherichia coli. Mol Microbiol. 84, 36-50 (2012).
51. Bordeau, V. & Felden, B. Curli synthesis and biofilm formation in enteric bacteria are controlled by a dynamic small RNA module made up of a pseudoknot assisted by an RNA chaperone. Nucleic Acids Res. 42, 4682-4696 (2014).
52. Ogasawara, H., Yamamoto, K. & Ishihama, A. Role of the biofilm master regulator CsgD in cross-regulation between biofilm formation and flagellar synthesis. J Bacteriol. 193, 2587-2597 (2011).
53. Mika, F. et al. Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Mol Microbiol. 84, 51-65 (2012).
54. Thomason, M. K., Fontaine, F., De Lay, N. & Storz, G. A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. Mol Microbiol. 84, 17-35 (2012).
55. Chevance, F. F. V. & Hughes, K. T. Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol. 6, 455-465 (2008).
56. Itoh, Y. et al. Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-beta-1,6-N-acetyl-D-glucosamine. J Bacteriol. 190, 3670-3680 (2008).
57. Liu, M. Y. et al. The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J Biol Chem. 272, 17502-17510 (1997).
58. Wang, X. et al. CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol Microbiol. 56, 1648-1663 (2005).
59. Weilbacher, T. et al. A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol Microbiol. 48, 657-670 (2003).
60. Claudia, M. et al. Hfq and Hfq-dependent small RNAs are major contributors to multicellular development in Salmonella enterica serovar typhimurium. RNA Biol. 9, 489-502 (2012).
61. Barker, C. S., Pru, B. M. & Matsumura, P. Increased Motility of Escherichia coli by Insertion Sequence Element Integration into the Regulatory Region of the flhD Operon. J Bacteriol. 186, 7529-7537 (2004).
62. Jackson, D. W. et al. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol. 184, 290-301 (2002).
63. Ito, A., May, T., Taniuchi, A., Kawata, K. & Okabe, S. Localized expression profiles of rpoS in Escherichia coli biofilms. Biotechnol Bioeng. 103, 975-983 (2009).
64. Ferrieres, L., Thompson, A. & Clarke, D. J. Elevated levels of sigma S inhibit biofilm formation in Escherichia coli: a role for the Rcs phosphorelay. Microbiology. 155, 3544-3553 (2009).
65. Adams, J. L. & McLean, R. J. Impact of rpoS deletion on Escherichia coli biofilms. Appl Env Microbiol. 65, 4285-4287 (1999).
66. Bak, G., Han, K., Kim, D. & Lee, Y. Roles of rpoS-activating small RNAs in pathways leading to acid resistance of Escherichia coli. Microbiologyopen. 3, 15-28 (2014).
67. Jorgensen, M. G. et al. Small regulatory RNAs control the multi-cellular adhesive lifestyle of Escherichia coli. Mol Microbiol. 84, 36-50 (2012).
68. Baba, T. et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2, 2006 0008 (2006).
69. Han, K., Kim, K. S., Bak, G., Park, H. & Lee, Y. Recognition and discrimination of target mRNAs by Sib RNAs, a cis-encoded sRNA family. Nucleic Acids Res. 38, 5851-5866 (2010).
70. Kim, S., Kim, H., Park, I. & Lee, Y. Mutational analysis of RNA structures and sequences postulated to affect 3′ processing of M1 RNA, the RNA component of Escherichia coli RNase P. J Biol Chem. 271, 19330-19337 (1996).
71. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97, 6640-6645 (2000).
72. Bak, G., Han, K., Kim, K. & Lee, Y. Electrophoretic mobility shift assay of RNA-RNA complexes. Methods Mol Biol. 1240, 153-163 (2015).
73. Zhang, X. & Bremer, H. Control of the Escherichia coli rrnB P1 promoter strength by ppGpp. J Biol Chem. 270, 11181-11189 (1995).