Spot 42 small RNA regulates arabinose-inducible araBAD promoter activity by repressing synthesis of the high-affinity low-capacity arabinose transporter

Journal of Bacteriology

Volumn 199, Issue 3, 2017, Pages

  Chen, Jiandong ^a   Gottesman, Susan ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Arabinose transporter; Arabinose inducible promoter; Posttranscriptional regulation; Regulatory small RNA

Indexed keywords

ARABINOSE; ARAFGH PROTEIN; CARRIER PROTEIN; CYCLIC AMP; MESSENGER RNA; RECEPTOR PROTEIN; RNA; SPOT 42 SMALL RNA; UNCLASSIFIED DRUG;

ARABAD GENE; ARAF GENE; ARTICLE; BASE PAIRING; BINDING AFFINITY; CATABOLITE REPRESSION; COMPLEX FORMATION; CONTROLLED STUDY; ESCHERICHIA COLI; GENE; GENE EXPRESSION REGULATION; GENE REPRESSION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; SYNTHESIS; TRANSCRIPTION REGULATION;

EID: 85011300276     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00691-16     Document Type: Article

References (38)

1. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121-4130. https://doi.org/10.1128/jb.177.14.4121-4130.1995.
2. Schleif R. 2010. AraC protein, regulation of the L-arabinose operon in Escherichia coli, and the light switch mechanism of AraC action. FEMS Microbiol Rev 34:779-796. https://doi.org/10.1111/j.1574-6976.2010.00226.x.
3. Hogg RW. 1977. L-Arabinose transport and the L-arabinose binding protein of Escherichia coli. J Supramol Struct 6:411-417. https://doi.org/10.1002/jss.400060314.
4. Siegele DA, Hu JC. 1997. Gene expression from plasmids containing the araBAD promoter at subsaturating inducer concentrations represents mixed populations. Proc Natl Acad Sci U S A 94:8168-8172. https://doi.org/10.1073/pnas.94.15.8168.
5. Khlebnikov A, Risa O, Skaug T, Carrier TA, Keasling JD. 2000. Regulatable arabinose-inducible gene expression system with consistent control in all cells of a culture. J Bacteriol 182:7029-7034. https://doi.org/10.1128/JB.182.24.7029-7034.2000.
6. Khlebnikov A, Datsenko KA, Skaug T, Wanner BL, Keasling JD. 2001. Homogeneous expression of the P(BAD) promoter in Escherichia coli by constitutive expression of the low-affinity high-capacity AraE transporter. Microbiology 147:3241-3247. https://doi.org/10.1099/00221287-147-12-3241.
7. Afroz T, Biliouris K, Boykin KE, Kaznessis Y, Beisel CL. 2015. Trade-offs in engineering sugar utilization pathways for titratable control. ACS Synth Biol 4:141-149. https://doi.org/10.1021/sb400162z.
8. Gottesman S, Storz G. 2011. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 3:pii=a003798. https://doi.org/10.1101/cshperspect.a003798.
9. Storz G, Vogel J, Wassarman KM. 2011. Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43:880-891. https://doi.org/10.1016/j.molcel.2011.08.022.
10. Updegrove TB, Zhang A, Storz G. 2016. Hfq: the flexible RNA matchmaker. Curr Opin Microbiol 30:133-138. https://doi.org/10.1016/j.mib.2016.02.003.
11. Vogel J, Luisi BF. 2011. Hfq and its constellation of RNA. Nat Rev Microbiol 9:578-589. https://doi.org/10.1038/nrmicro2615.
12. Sahagan BG, Dahlberg JE. 1979. A small, unstable RNA molecule of Escherichia coli: spot 42 RNA. II. Accumulation and distribution. J Mol Biol 131:593-605.
13. 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. https://doi.org/10.1016/j.molcel.2010.12.027.
14. Hansen GA, Ahmad R, Hjerde E, Fenton CG, Willassen NP, Haugen P. 2012. Expression profiling reveals Spot 42 small RNA as a key regulator in the central metabolism of Aliivibrio salmonicida. BMC Genomics 13:37. https://doi.org/10.1186/1471-2164-13-37.
15. Beisel CL, Updegrove TB, Janson BJ, Storz G. 2012. Multiple factors dictate target selection by Hfq-binding small RNAs. EMBO J 31: 1961-1974. https://doi.org/10.1038/emboj.2012.52.
16. Mandin P, Gottesman S. 2010. Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 29:3094-3107. https://doi.org/10.1038/emboj.2010.179.
17. Mandin P. 2012. Genetic screens to identify bacterial sRNA regulators. Methods Mol Biol 905:41-60. https://doi.org/10.1007/978-1-61779-949-5_4.
18. De Lay N, Gottesman S. 2012. A complex network of small non-coding RNAs regulate motility in Escherichia coli. Mol Microbiol 86:524-538. https://doi.org/10.1111/j.1365-2958.2012.08209.x.
19. Lee HJ, Gottesman S. 2016. sRNA roles in regulating transcriptional regulators: Lrp and SoxS regulation by sRNAs. Nucleic Acids Res 44: 6907-6923. https://doi.org/10.1093/nar/gkw358.
20. Parker A, Gottesman S. 2016. Small RNA regulation of TolC, the outer membrane component of bacterial multidrug transporters. J Bacteriol 198:1101-1113. https://doi.org/10.1128/JB.00971-15.
21. Cox MM. 2003. The bacterial RecA protein as a motor protein. Annu Rev Microbiol 57:551-577. https://doi.org/10.1146/annurev.micro.57.030502.090953.
22. Bak G, Lee J, Suk S, Kim D, Young Lee J, Kim KS, Choi BS, Lee Y. 2015. Identification of novel sRNAs involved in biofilm formation, motility, and fimbriae formation in Escherichia coli. Sci Rep 5:15287. https://doi.org/10.1038/srep15287.
23. Zhang A, Schu DJ, Tjaden BC, Storz G, Gottesman S. 2013. Mutations in interaction surfaces differentially impact E. coli Hfq association with small RNAs and their mRNA targets. J Mol Biol 425:3678-3697. https://doi.org/10.1016/j.jmb.2013.01.006.
24. Jensen PR, Hammer K. 1998. The sequence of spacers between the consensus sequences modulates the strength of prokaryotic promoters. Appl Environ Microbiol 64:82-87.
25. Wright PR, Richter AS, Papenfort K, Mann M, Vogel J, Hess WR, Backofen R, Georg J. 2013. Comparative genomics boosts target prediction for bacterial small RNAs. Proc Natl Acad Sci U S A 110:E3487-E3496. https://doi.org/10.1073/pnas.1303248110.
26. Moon K, Gottesman S. 2011. Competition among Hfq-binding small RNAs in Escherichia coli. Mol Microbiol 82:1545-1562. https://doi.org/10.1111/j.1365-2958.2011.07907.x.
27. Møller T, Franch T, Udesen C, Gerdes K, Valentin-Hansen P. 2002. Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev 16:1696-1706. https://doi.org/10.1101/gad.231702.
28. Qiu D, Damron FH, Mima T, Schweizer HP, Yu HD. 2008. PBAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl Environ Microbiol 74:7422-7426. https://doi.org/10.1128/AEM.01369-08.
29. Morgan-Kiss RM, Wadler C, Cronan JE, Jr. 2002. Long-term and homogeneous regulation of the Escherichia coli araBAD promoter by use of a lactose transporter of relaxed specificity. Proc Natl Acad Sci U S A 99:7373-7377. https://doi.org/10.1073/pnas.122227599.
30. Afroz T, Biliouris K, Kaznessis Y, Beisel CL. 2014. Bacterial sugar utilization gives rise to distinct single-cell behaviours. Mol Microbiol 93:1093-1103. https://doi.org/10.1111/mmi.12695.
31. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
32. Mandin P, Gottesman S. 2009. A genetic approach for finding small RNAs regulators of genes of interest identifies RybC as regulating the DpiA/DpiB two-component system. Mol Microbiol 72:551-565. https://doi.org/10.1111/j.1365-2958.2009.06665.x.
33. Court DL, Swaminathan S, Yu D, Wilson H, Baker T, Bubunenko M, Sawitzke J, Sharan SK. 2003. Mini-lambda: a tractable system for chromosome and BAC engineering. Gene 315:63-69. https://doi.org/10.1016/S0378-1119(03)00728-5.
34. Chung CT, Niemela SL, Miller RH. 1989. One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc Natl Acad Sci U S A 86:2172-2175. https://doi.org/10.1073/pnas.86.7.2172.
35. 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. https://doi.org/10.1073/pnas.95.21.12462.
36. Zhou Y, Gottesman S. 1998. Regulation of proteolysis of the stationaryphase sigma factor RpoS. J Bacteriol 180:1154-1158.
37. Massé E, Escorcia FE, Gottesman S. 2003. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 17:2374-2383. https://doi.org/10.1101/gad.1127103.
38. De Lay N, Gottesman S. 2009. The Crp-activated small noncoding regulatory RNA CyaR (RyeE) links nutritional status to group behavior. J Bacteriol 191:461-476. https://doi.org/10.1128/JB.01157-08.