Genome-wide analysis of phosphorylated PhoP binding to chromosomal DNA reveals several novel features of the PhoPR-mediated phosphate limitation response in Bacillus subtilis

Journal of Bacteriology

Volumn 197, Issue 8, 2015, Pages 1492-1506

  Salzberg, Letal I ^a   Botella, Eric ^a   Hokamp, Karsten ^a   Antelmann, Haike ^b   Maaß, Sandra ^b   Becher, Dörte ^b   Noone, David ^a   Devine, Kevin M ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; COMQ PROTEIN; DNA FRAGMENT; GGAA PROTEIN; GLPQ PROTEIN; PEPTIDOGLYCAN; PGSB PROTEIN; PHOB PROTEIN; PHOD PROTEIN; PHOP PROTEIN; PHOR PROTEIN; PHOSPHATASE; PHOSPHATE; PSTS PROTEIN; RAPK PROTEIN; TAGA PROTEIN; TEICHOIC ACID; TRANSCRIPTOME; TUAA PROTEIN; UNCLASSIFIED DRUG; WAPA PROTEIN; YJDB PROTEIN; YKOL PROTEIN; YOMG PROTEIN; YQGS PROTEIN; YURI PROTEIN; YVYD PROTEIN; YYDBCD PROTEIN; BACTERIAL PROTEIN; BACTERIAL RNA; PHOP PROTEIN, BACTERIA; PROTEIN BINDING;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL WALL; BACTERIAL CHROMOSOME; CELL MEMBRANE; CHROMATIN IMMUNOPRECIPITATION; CYTOPLASM; OPERON; PRIORITY JOURNAL; PROTEIN BINDING; REGULON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; AMINO ACID SEQUENCE; BACTERIAL GENOME; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PHYSIOLOGY;

BACILLUS SUBTILIS; FIRMICUTES;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; OPERON; PHOSPHATES; PHOSPHORYLATION; PROTEIN BINDING; RNA, BACTERIAL;

EID: 84925989956     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02570-14     Document Type: Article

References (47)

1. Hsieh YJ, Wanner BL. 2010. Global regulation by the seven-component Pi signaling system. Curr Opin Microbiol 13:198-203. http://dx.doi.org /10.1016/j.mib.2010.01.014.
2. Botella E, Devine SK, Hubner S, Salzberg LI, Gale RT, Brown ED, Link H, Sauer U, Codée JD, Noone D, Devine KM. 2014. PhoR autokinase activity is controlled by an intermediate in wall teichoic acid metabolism that is sensed by the intracellular PAS domain during the PhoPRmediated phosphate limitation response of Bacillus subtilis. Mol Microbiol 94:1242-1259. http://dx.doi.org/10.1111/mmi.12833.
3. Vollmer W, Blanot D, de Pedro MA. 2008. Peptidoglycan structure and architecture. FEMS Microbiol Rev 32:149-167. http://dx.doi.org/10.1111 /j.1574-6976.2007.00094.x.
4. Weidenmaier C, Peschel A. 2008. Teichoic acids and related cell wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6:276-287. http://dx.doi.org/10.1038/nrmicro1861.
5. VanBogelen RA, Olson ER, Wanner BL, Neidhardt FC. 1996. Global analysis of proteins synthesized during phosphorus restriction in Escherichia coli. J Bacteriol 178:4344-4366.
6. Antelmann H, Tjalsma H, Voigt B, Ohlmeier S, Bron S, van Dijl JM, Hecker M. 2001. A proteomic view on genome-based signal peptide predictions. Genome Res 11:1484-1502. http://dx.doi.org/10.1101/gr.182801.
7. Allenby NE, O'Connor N, Prágai Z, Ward AC, Wipat A, Harwood CR. 2005. Genome-wide transcriptional analysis of the phosphate starvation stimulon of Bacillus subtilis. J Bacteriol 187:8063-8080. http://dx.doi.org /10.1128/JB.187.23.8063-8080.2005.
8. Baek JH, Lee SY. 2007. Transcriptome analysis of phosphate starvation response in Escherichia coli. J Microbiol Biotechnol 17:244-252.
9. Botella E, Hübner S, Hokamp K, Hansen A, Bisicchia P, Noone D, Powell L, Salzberg LI, Devine KM. 2011. Cell envelope gene expression in phosphate-limited Bacillus subtilis cells. Microbiology 157:2470-2484. http://dx.doi.org/10.1099/mic.0.049205-0.
10. Yang C, Huang TW, Wen SY, Chang CY, Tsai SF, Wu WF, Chang CH. 2012. Genome-wide PhoB binding and gene expression profiles reveal the hierarchical gene regulatory network of phosphate starvation in Escherichia coli. PLoS One 7:e47314. http://dx.doi.org/10.1371/journal.pone.0047314.
11. Hulett FM. 2002. The Pho regulon, p 193-201. In Sonenshein, AL, Hoch JA, Losick R (ed), Bacillus subtilis and its closest relatives. American Society for Microbiology Press, Washington, DC.
12. Liu W, Hulett FM. 1998. Comparison of PhoP binding to the tuaA promoter with PhoP binding to other Pho-regulon promoters establishes a Bacillus subtilis Pho core binding site. Microbiology 144:1443-1450. http://dx.doi.org/10.1099/00221287-144-5-1443.
13. Liu W, Eder S, Hulett FM. 1998. Analysis of Bacillus subtilis tagAB and tagDEF expression during phosphate starvation identifies a repressor role for PhoP-P J Bacteriol 180:753-758.
14. Soldo B, Lazarevic V, Pagni M, Karamata D. 1999. Teichuronic acid operon of Bacillus subtilis 168. Mol Microbiol 31:795-805.
15. Lahooti M, Harwood CR. 1999. Transcriptional analysis of the Bacillus subtilis teichuronic acid operon. Microbiology 145:3409-3417.
16. Bhavsar AP, Erdman LK, Schertzer JW, Brown ED. 2004. Teichoic acid is an essential polymer in Bacillus subtilis that is functionally distinct from teichuronic acid. J Bacteriol 186:7865-7873. http://dx.doi.org/10.1128/JB.186.23.7865-7873.2004.
17. Prágai Z, Allenby NE, O'Connor N, Dubrac S, Rapoport G, Msadek T, Harwood CR. 2004. Transcriptional regulation of the phoPR operon in Bacillus subtilis. J Bacteriol 186:1182-1190. http://dx.doi.org/10.1128/JB.186.4.1182-1190.2004.
18. Howell A, Dubrac S, Andersen KK, Noone D, Fert J, Msadek T, Devine KM. 2003. Genes controlled by the essential YycG/YycF two-component system of Bacillus subtilis revealed through a novel hybrid regulator approach. Mol Microbiol 49:1639-1655. http://dx.doi.org/10.1046/j.1365-2958.2003.03661.x.
19. Bisicchia P, Noone D, Lioliou E, Howell A, Quigley S, Jensen T, Jarmer H, Devine KM. 2007. The essential YycFG two-component system controls cell wall metabolism in Bacillus subtilis. Mol Microbiol 65:180-200. http://dx.doi.org/10.1111/j.1365-2958.2007.05782.x.
20. Bisicchia P, Lioliou E, Noone D, Salzberg LI, Botella E, Hübner S, Devine KM. 2010. Peptidoglycan metabolism is controlled by the WalRK (YycFG) and PhoPR two-component systems in phosphate-limited Bacillus subtilis cells. Mol Microbiol 75:972-989. http://dx.doi.org/10.1111/j.1365-2958.2009.07036.x.
21. Salzberg LI, Powell L, Hokamp K, Botella E, Noone D, Devine KM. 2013. The WalRK (YycFG) and σ(I) RsgI regulators cooperate to control CwlO and LytE expression in exponentially growing and stressed Bacillus subtilis cells. Mol Microbiol 87:180-195. http://dx.doi.org/10.1111/mmi.12092.
22. Law J, Buist G, Haandrikman A, Kok J, Venema G, Leenhouts K. 1995. A system to generate chromosomal mutations in Lactococcus lactis which allows fast analysis of targeted genes. J Bacteriol 177:7011-7018.
23. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Müller JP, An Z, Merad T, Hancock IC, Harwood CR. 1997. Influence of Bacillus subtilis phoR on cell wall anionic polymers. Microbiology 143: 947-956. http://dx.doi.org/10.1099/00221287-143-3-947.
25. Wach A. 1996. PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in Saccharomyces cerevisiae. Yeast 12:259-265. http://dx.doi.org/10.1002/(SICI)1097-0061(19960315)12:3<259::AID-YEA901>3.0.CO;2-C.
26. Bloor AE, Cranenburgh RM. 2006. An efficient method of selectable marker gene excision by Xer recombination for gene replacement in bacterial chromosomes. Appl Environ Microbiol 72:2520-2525. http://dx.doi.org/10.1128/AEM.72.4.2520-2525.2006.
27. Guérout-Fleury AM, Shazand K, Frandsen N, Stragier P. 1995. Antibiotic-resistance cassettes for Bacillus subtilis. Gene 167:335-336. http://dx.doi.org/10.1016/0378-1119(95)00652-4.
28. Bisicchia P, Botella E, Devine KM. 2010. Suite of novel vectors for ectopic insertion of GFP, CFP, and IYFP transcriptional fusions in single copy at the amyE and bglS loci in Bacillus subtilis. Plasmid 64:143-149. http://dx.doi.org/10.1016/j.plasmid.2010.06.002.
29. Botella E, Fogg M, Jules M, Piersma S, Doherty G, Hansen A, Denham EL, Le Chat L, Veiga P, Bailey K, Lewis PJ, van Dijl JM, Aymerich S, Wilkinson AJ, Devine KM. 2010. pBaSysBioII: an integrative plasmid generating gfp transcriptional fusions for high-throughput analysis of gene expression in Bacillus subtilis. Microbiology 156:1600-1608. http: //dx.doi.org/10.1099/mic.0.035758-0.
30. Bhavsar AP, Zhao X, Brown ED. 2001. Development and characterization of a xylose-dependent system for expression of cloned genes in Bacillus subtilis: conditional complementation of a teichoic acid mutant. Appl Environ Microbiol 67:403-410. http://dx.doi.org/10.1128/AEM.67.1.403-410.2001.
31. Yamamoto H, Kurosawa S, Sekiguchi J. 2003. Localization of the vegetative cell wall hydrolases LytC, LytE, and LytF on the Bacillus subtilis cell surface and stability of these enzymes to cell wall-bound or extracellular proteases. J Bacteriol 185:6666-6677. http://dx.doi.org/10.1128/JB.185.22.6666-6677.2003.
32. Rasmussen S, Nielsen HB, Jarmer H. 2009. The transcriptionally active regions in the genome of Bacillus subtilis. Mol Microbiol 73:1043-1057. http://dx.doi.org/10.1111/j.1365-2958.2009.06830.x.
33. Toedling J, Skylar O, Krueger T, Fischer JJ, Sperling S, Huber W. 2007. Ringo: an R/Bioconductor package for analyzing ChIP-chip readouts. BMC Bioinformatics 8:221. http://dx.doi.org/10.1186/1471-2105-8-221.
34. Noone D, Howell A, Devine KM. 2000. Expression of ykdA, encoding a Bacillus subtilis homologue of HtrA, is heat shock inducible and negatively autoregulated. J Bacteriol 182:1592-1599. http://dx.doi.org/10.1128/JB.182.6.1592-1599.2000.
35. -ΔΔCT method. Methods 25: 402-408. http://dx.doi.org/10.1006/meth.2001.1262.
36. Howell A, Dubrac S, Noone D, Varughese KI, Devine KM. 2006. Interactions between the YycFG and PhoPR two-component systems in Bacillus subtilis: the PhoR kinase phosphorylates the non-cognate YycF response regulator upon phosphate limitation. Mol Microbiol 59:1199-1215. http://dx.doi.org/10.1111/j.1365-2958.2005.05017.x.
37. Chi BK, Gronau K, Mäder U, Hessling B, Becher D, Antelmann H. 2011. S-bacillithiolation protects against hypochlorite stress in Bacillus subtilis as revealed by transcriptomics and redox proteomics. Mol Cell Proteomics 10:M111.009506. http://dx.doi.org/10.1074/mcp.M111.009506.
38. Barbe V, Cruveiller S, Kunst F, Lenoble P, Meurice G, Sekowska A, Vallenet D, Wang T, Moszer I, Médigue C, Danchin A. 2009. From a consortium sequence to a unified sequence: the Bacillus subtilis 168 reference genome a decade later. Microbiology 155:1758-1775. http://dx.doi.org/10.1099/mic.0.027839-0.
39. Uniprot Consortium. 2007. The Universal Protein Resource (UniProt). Nucleic Acids Res 35(database issue):D193-D197. http://dx.doi.org/10.1093/nar/gkl929.
40. Paul S, Birkey S, Liu W, Hulett FM. 2004. Autoinduction of Bacillus subtilis phoPR operon transcription results from enhanced transcription from EσA-and EσE-responsive promoters by phosphorylated PhoP. J Bacteriol 186:4262-4275. http://dx.doi.org/10.1128/JB.186.13.4262-4275.2004.
41. Nicolas P, Mäder U, Dervyn E, Rochat T, Leduc A, Pigeonneau N, Bidnenko E, Marchadier E, Hoebeke M, Aymerich S, Becher D, Bisicchia P, Botella E, Delumeau O, Doherty G, Denham EL, Fogg MJ, Fromion V, Goelzer A, Hansen A, Härtig E, Harwood CR, Homuth G, Jarmer H, Jules M, Klipp E, Le Chat L, Lecointe F, Lewis P, Liebermeister W, March A, Mars RA, Nannapaneni P, Noone D, Pohl S, Rinn B, Rügheimer F, Sappa PK, Samson F, Schaffer M, Schwikowski B, Steil L, Stülke J, Wiegert T, Devine KM, Wilkinson AJ, van Dijl JM, Hecker M, Völker U, Bessières P, Noirot P. 2012. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335:1103-1106. http://dx.doi.org/10.1126/science.1206848.
42. Hulett FM, Lee J, Shi L, Sun G, Chesnut R, Sharkova E, Duggan MF, Kapp N. 1994. Sequential action of two-component genetic switches regulates the PHO regulon in Bacillus subtilis. J Bacteriol 176:1348-1358.
43. 54-dependent transcription. FEMS Microbiol Rev 35:425-440. http://dx.doi.org/10.1111/j.1574-6976.2010.00255.x.
44. Lee DJ, Minchin SD, Busby SJW. 2012. Activating transcription in bacteria. Annu Rev Microbiol 66:125-152. http://dx.doi.org/10.1146/annurev-micro-092611-150012.
45. Belitsky BR, Sonenshein AL. 1999. An enhancer element located downstream of the major glutamate dehydrogenase gene of Bacillus subtilis. Proc Natl Acad SciUSA 96:10290-10295. http://dx.doi.org/10.1073/pnas.96.18.10290.
46. 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.
47. Maguin E, Duwat P, Hege T, Ehrlich SD, Gruss A. 1992. New thermosensitive plasmid for gram-positive bacteria. J Bacteriol 174:5633-5638.