Genome-scale analyses of Escherichia coli and Salmonella enterica AraC reveal noncanonical targets and an expanded core regulon

Journal of Bacteriology

Volumn 196, Issue 3, 2014, Pages 660-671

  Stringer, Anne M ^a   Currenti, Salvatore ^b   Bonocora, Richard P ^a   Baranowski, Catherine ^a   Petrone, Brianna L ^a   Palumbo, Michael J ^a   Reilly, Andrew A ^a   Zhang, Zhen ^a   Erill, Ivan ^c   Wade, Joseph T ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOSE; ARAC PROTEIN; RHO FACTOR;

ARAD GENE; ARAE GENE; ARTICLE; BACTERIAL GENE; BINDING SITE; BIOINFORMATICS; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GENE ACTIVATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE MAPPING; GENE REGULATORY NETWORK; GENE REPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; GENOME ANALYSIS; GENOMICS; NONHUMAN; POLB GENE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; REGULATOR GENE; REGULON; RNA SEQUENCE; SALMONELLA ENTERICA; SPECIES COMPARISON; TRANSCRIPTION REGULATION; YDEM GENE; YDEN GENE; YGEA GENE; YTFQ GENE;

ARABINOSE; ARAC TRANSCRIPTION FACTOR; BASE SEQUENCE; BINDING SITES; CHROMOSOME MAPPING; DNA, BACTERIAL; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; REGULON; SALMONELLA ENTERICA;

EID: 84892388084     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01007-13     Document Type: Article

References (56)

1. Egan SM. 2002. Growing repertoire of AraC/XylS activators. J. Bacteriol. 184:5529-5532. http://dx.doi.org/10.1128/JB.184.20.5529-5532.2002.
2. Gross J, Englesberg E. 1959. Determination of the order of mutational sites governing L-arabinose utilization in Escherichia coli B/r bv transduction with phage Plbt. Virology 9:314-331. http://dx.doi.org/10.1016/0042-6822(59)90125-4.
3. Englesberg E, Irr J, Power J, Lee N. 1965. Positive control of enzyme synthesis by gene C in the L-arabinose system. J. Bacteriol. 90:946-957.
4. Greenblatt J, Schleif R. 1971. Arabinose C protein: regulation of the arabinose operon in vitro. Nat. New Biol. 233:166-170.
5. 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. http://dx.doi.org/10.1111/j.1574-6976.2010.00226.x.
6. Dunn TM, Hahn S, Ogden S, Schleif RF. 1984. An operator at -280 base pairs that is required for repression of araBAD operon promoter: addition of DNA helical turns between the operator and promoter cyclically hinders repression. Proc. Natl. Acad. Sci. U. S. A. 81:5017-5020. http://dx.doi.org/10.1073/pnas.81.16.5017.
7. Wade JT, Struhl K, Busby SJ, Grainger DC. 2007. Genomic analysis of protein-DNA interactions in bacteria: insights into transcription and chromosome organization. Mol. Microbiol. 65:21-26. http://dx.doi.org/10.1111/j.1365-2958.2007.05781.x.
8. Grainger DC, Aiba H, Hurd D, Browning DF, Busby SJ. 2007. Transcription factor distribution in Escherichia coli: studies with FNR protein. Nucleic Acids Res. 35:269-278. http://dx.doi.org/10.1093/nar/gkl1023.
9. Shimada T, Ishihama A, Busby SJ, Grainger DC. 2008. The Escherichia coli RutR transcription factor binds at targets within genes as well as intergenic regions. Nucleic Acids Res. 36:3950-3955. http://dx.doi.org/10.1093/nar/gkn339.
10. Bonocora RP, Fitzgerald DM, Stringer AM, Wade JT. 2013. Noncanonical protein-DNA interactions identified by ChIP are not artifacts. BMC Genomics 14:254. http://dx.doi.org/10.1186/1471-2164-14-254.
11. Rhodius VA, Wade JT. 2009. Technical considerations in using DNA microarrays to define regulons. Methods 47:63-72. http://dx.doi.org/10.1016/j.ymeth.2008.10.017.
12. Perez JC, Groisman EA. 2009. Evolution of transcriptional regulatory circuits in bacteria. Cell 138:233-244. http://dx.doi.org/10.1016/j.cell.2009.07.002.
13. Perez JC, Shin D, Zwir I, Latifi T, Hadley TJ, Groisman EA. 2009. Evolution of a bacterial regulon controlling virulence and Mg(2+) homeostasis. PLoS Genet. 5:e1000428. http://dx.doi.org/10.1371/journal.pgen.1000428.
14. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
15. Butland G, Peregrin-Alvarez JM, Li J, Yang W, Yang X, Canadien V, Starostine A, Richards D, Beattie B, Krogan N, Davey M, Parkinson J, Greenblatt J, Emili A. 2005. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433:531-537. http://dx.doi.org/10.1038/nature03239.
16. Cherepanov PP, Wackernagel W. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14. http://dx.doi.org/10.1016/0378-1119(95)00193-A.
17. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008. http://dx.doi.org/10.1038/msb4100050.
18. Stringer AM, Singh N, Yermakova A, Petrone BL, Amarasinghe JJ, Reyes-Diaz L, Mantis NJ, Wade JT. 2012. FRUIT, a scar-free system for targeted chromosomal mutagenesis, epitope tagging, and promoter replacement in Escherichia coli and Salmonella enterica. PLoS One 7:e44841. http://dx.doi.org/10.1371/journal.pone.0044841.
19. Horton RM, Cai Z, Ho SN, Pease L. 1990. Gene splicing by overlap extension: tailor made genes using the polymerase chain reaction. Biotechniques 8:528-535.
20. Dornenburg JE, DeVita AM, Palumbo MJ, Wade JT. 2010. Widespread antisense transcription in Escherichia coli. mBio 1:e00024-10. http://dx.doi.org/10.1128/mBio.00024-10.
21. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680. http://dx.doi.org/10.1093/nar/22.22.4673.
22. Schneider TD, Stormo GD, Gold L, Ehrenfeucht A. 1986. Information content of binding sites on nucleotide sequences. J. Mol. Biol. 188:415-431. http://dx.doi.org/10.1016/0022-2836(86)90165-8.
23. Church G, Gilbert W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. U. S. A. 81:1991-1995. http://dx.doi.org/10.1073/pnas.81.7.1991.
24. Lew JM, Mao C, Shukla M, Warren A, Will R, Kuznetsov D, Xenarios I, Robertson BD, Gordon SV, Schnappinger D, Cole ST, Sobral B. 2013. Database resources for the tuberculosis community. Tuberculosis 93:12-17. http://dx.doi.org/10.1016/j.tube.2012.11.003.
25. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. http://dx.doi.org/10.1186/gb-2009-10-3-r25.
26. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28:511-515. http://dx.doi.org/10.1038/nbt.1621.
27. Kosiba BE, Schleif R. 1982. Arabinose-inducible promoter from Escherichia coli. Its cloning from chromosomal DNA, identification as the araFG promoter and sequence. J. Mol. Biol. 156:53-66.
28. Novotny CP, Englesberg E. 1966. The L-arabinose permease system in Escherichia coli B/r. Biochim. Biophys. Acta 117:217-230. http://dx.doi.org/10.1016/0304-4165(66)90169-3.
29. Brown CE, Hogg RW. 1972. A second transport system for L-arabinose in Escherichia coli B-r controlled by the araC gene. J. Bacteriol. 111:606-613.
30. Stoner C, Schleif R. 1983. The araE low affinity L-arabinose transport promoter. Cloning, sequence, transcription start site and DNA binding sites of regulatory proteins. J. Mol. Biol. 171:369-381.
31. Hendrickson W, Stoner C, Schleif R. 1990. Characterization of the Escherichia coli araFGH and araJ promoters. J. Mol. Biol. 215:497-510. http://dx.doi.org/10.1016/S0022-2836(05)80163-9.
32. Hamilton EP, Lee N. 1988. Three binding sites for AraC protein are required for autoregulation of araC in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 85:1749-1753. http://dx.doi.org/10.1073/pnas.85.6.1749.
33. Lee N, Francklyn C, Hamilton EP. 1987. Arabinose-induced binding of AraC protein to araI2 activates the araBAD operon promoter. Proc. Natl. Acad. Sci. U. S. A. 84:8814-8818. http://dx.doi.org/10.1073/pnas.84.24.8814.
34. Lu Y, Flaherty C, Hendrickson W. 1992. AraC protein contacts asymmetric sites in the Escherichia coli araFGH promoter. J. Biol. Chem. 267:24848-24857.
35. Bailey TL, Elkan C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2:28-36.
36. Desai TA, Rao CV. 2010. Regulation of arabinose and xylose metabolism in Escherichia coli. Appl. Environ. Microbiol. 76:1524-1532. http://dx.doi.org/10.1128/AEM.01970-09.
37. Hemm MR, Paul BJ, Schneider TD, Storz G, Rudd KE. 2008. Small membrane proteins found by comparative genomics and ribosome binding site models. Mol. Microbiol. 70:1487-1501. http://dx.doi.org/10.1111/j.1365-2958.2008.06495.x.
38. Cho BK, Zengler K, Qiu Y, Park YS, Knight EM, Barrett CL, Gao Y, Palsson BØ. 2009. The transcription unit architecture of the Escherichia coli genome. Nat. Biotechnol. 27:1043-1049. http://dx.doi.org/10.1038/nbt.1582.
39. Horler RS, Müller A, Williamson DC, Potts JR, Wilson KS, Thomas GH. 2009. Furanose-specific sugar transport: characterization of a bacterial galactofuranose-binding protein. J. Biol. Chem. 284:31156-31163. http://dx.doi.org/10.1074/jbc.M109.054296.
40. Gardner PP, Barquist L, Bateman A, Nawrocki EP, Weinberg Z. 2011. RNIE: genome-wide prediction of bacterial intrinsic terminators. Nucleic Acids Res. 39:5845-5852. http://dx.doi.org/10.1093/nar/gkr168.
41. Burr T, Mitchell J, Kolb A, Minchin S, Busby S. 2000. DNA sequence elements located immediately upstream of the -10 hexamer in Escherichia coli promoters: a systematic study. Nucleic Acids Res. 28:1864-1870. http://dx.doi.org/10.1093/nar/28.9.1864.
42. Lucchini S, Rowley G, Goldberg MD, Hurd D, Harrison M, Hinton JC. 2006. H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog. 2:e81. http://dx.doi.org/10.1371/journal.ppat.0020081.
43. Irani MH, Orosz L, Adhya S. 1983. A control element within a structural gene: the gal operon of Escherichia coli. Cell 32:783-788. http://dx.doi.org/10.1016/0092-8674(83)90064-8.
44. Bulyk ML, McGuire AM, Masuda N, Church GM. 2004. A motif cooccurrence approach for genome-wide prediction of transcription-factorbinding sites in Escherichia coli. Genome Res. 14:201-208. http://dx.doi.org/10.1101/gr.1448004.
45. Lee K, Zhan X, Gao J, Qiu J, Feng Y, Meganathan R, Cohen SN, Georgiou G. 2003. RraA, a protein inhibitor of RNase E activity that globally modulates RNA abundance in E. coli. Cell 114:623-634. http://dx.doi.org/10.1016/j.cell.2003.08.003.
46. Lesnik EA, Sampath R, Levene HB, Henderson TJ, McNeil JA, Ecker DJ. 2001. Prediction of Rho-independent transcriptional terminators in Escherichia coli. Nucleic Acids Res. 29:3583-3894. http://dx.doi.org/10.1093/nar/29.17.3583.
47. de Hoon MJ, Makita Y, Nakai K, Miyano S. 2005. Prediction of transcriptional terminators in Bacillus subtilis and related species. PLoS Comput. Biol. 1:e25. http://dx.doi.org/10.1371/journal.pcbi.0010025.
48. d'Aubenton-Carafa Y, Brody E, Thermes C. 1990. Prediction of Rhoindependent Escherichia coli transcription terminators. A statistical analysis of their RNA stem-loop structures. J. Mol. Biol. 216:835-858.
49. Kingsford CL, Ayanbule K, Salzberg SL. 2007. Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship toDNAuptake. Genome Biol. 8:R22. http://dx.doi.org/10.1186/gb-2007-8-2-r22.
50. Mitra A, Kesarwani AK, Pal D, Nagaraja V. 2011. WebGeSTer DB-a transcription terminator database. Nucleic Acids Res. 39:D129-D135. http://dx.doi.org/10.1093/nar/gkq971.
51. Reeder T, Schleif R. 1991. Mapping, sequence, and apparent lack of function of araJ, a gene of the Escherichia coli arabinose regulon. J. Bacteriol. 173:7765-7771.
52. Pham P, Rangarajan S, Woodgate R, Goodman MF. 2001. Roles of DNA polymerases V and II in SOS-induced error-prone and error-free repair in Escherichia coli. Proc. Nat. Acad. Sci. U. S. A. 98:8350-8354. http://dx.doi.org/10.1073/pnas.111007198.
53. Al Mamun AA. 2007. Elevated expression of DNA polymerase II increases spontaneous mutagenesis in Escherichia coli. Mutat. Res. 625:29-39. http://dx.doi.org/10.1016/j.mrfmmm.2007.05.002.
54. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188-1190. http://dx.doi.org/10.1101/gr.849004.
55. Blattner FR, Plunkett G, III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. 1997. The complete genome of Escherichia coli K-12. Science 277:1453-1474. http://dx.doi.org/10.1126/science.277.5331.1453.
56. Jarvik T, Smillie C, Groisman EA, Ochman H. 2010. Short-term signatures of evolutionary change in the Salmonella enterica serovar Typhimurium 14028 genome. J. Bacteriol. 192:560-567. http://dx.doi.org/10.1128/JB.01233-09.