Intermediate Levels of Bacillus subtilis CodY Activity Are Required for Derepression of the Branched-Chain Amino Acid Permease, BraB

PLoS Genetics

Volumn 11, Issue 10, 2015, Pages

  Belitsky, Boris R ^a   Brinsmade, Shaun R ^a,b   Sonenshein, Abraham L ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BRANCHED CHAIN AMINO ACID; PERMEASE; PERMEASE BRAB; REGULATOR PROTEIN CODY; REGULATOR PROTEIN SCOC; UNCLASSIFIED DRUG; AMINO ACID TRANSPORTER; DNA BINDING PROTEIN; PROTEIN BINDING; SCOC PROTEIN, BACILLUS SUBTILIS; TRANSCRIPTION FACTOR;

ARTICLE; BACILLUS SUBTILIS; BINDING SITE; CONTROLLED STUDY; ENZYME REPRESSION; ENZYME SYNTHESIS; NONHUMAN; POSITIVE FEEDBACK; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOGENICITY;

AMINO ACID TRANSPORT SYSTEMS; AMINO ACIDS, BRANCHED-CHAIN; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BINDING SITES; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION FACTORS;

EID: 84946600953     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005600     Document Type: Article

References (48)

1. Belitsky BR, Role of branched-chain amino acid transport in Bacillus subtilis CodY activity. J Bacteriol. 2015;197(8):1330–8. doi: 10.1128/JB.02563-14 25645558
2. Belitsky BR, Sonenshein AL, Contributions of multiple binding sites and effector-independent binding to CodY-mediated regulation in Bacillus subtilis. J Bacteriol. 2011;193(2):473–84. doi: 10.1128/JB.01151-10 21097623
3. Sonenshein AL, CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr Opin Microbiol. 2005;8(2):203–7. 15802253
4. Sonenshein AL, Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol. 2007;5(12):917–27. 17982469
5. Belitsky BR, Gustafsson MC, Sonenshein AL, Von Wachenfeldt C, An lrp-like gene of Bacillus subtilis involved in branched-chain amino acid transport. J Bacteriol. 1997;179(17):5448–57. 9287000
6. Molle V, Nakaura Y, Shivers RP, Yamaguchi H, Losick R, Fujita Y, et al. Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J Bacteriol. 2003;185(6):1911–22. 12618455
7. Belitsky BR, Sonenshein AL, Genome-wide identification of Bacillus subtilis CodY-binding sites at single-nucleotide resolution. Proc Natl Acad Sci U S A. 2013;110(17):7026–31. doi: 10.1073/pnas.1300428110 23569278
8. Brinsmade SR, Alexander EL, Livny J, Stettner AI, Segre D, Rhee KY, et al. Hierarchical expression of genes controlled by the Bacillus subtilis global regulatory protein CodY. Proc Natl Acad Sci USA. 2014;111(22):8227–32. doi: 10.1073/pnas.1321308111 24843172
9. Guedon E, Serror P, Ehrlich SD, Renault P, Delorme C, Pleiotropic transcriptional repressor CodY senses the intracellular pool of branched-chain amino acids in Lactococcus lactis. Mol Microbiol. 2001;40(5):1227–39. 11401725
10. Petranovic D, Guedon E, Sperandio B, Delorme C, Ehrlich D, Renault P, Intracellular effectors regulating the activity of the Lactococcus lactis CodY pleiotropic transcription regulator. Mol Microbiol. 2004;53(2):613–21. 15228538
11. Shivers RP, Sonenshein AL, Activation of the Bacillus subtilis global regulator CodY by direct interaction with branched-chain amino acids. Mol Microbiol. 2004;53(2):599–611. 15228537
12. Ratnayake-Lecamwasam M, Serror P, Wong KW, Sonenshein AL, Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev. 2001;15(9):1093–103. 11331605
13. Handke LD, Shivers RP, Sonenshein AL, Interaction of Bacillus subtilis CodY with GTP. J Bacteriol. 2008;190(3):798–806. 17993518
14. Brinsmade SR, Sonenshein AL, Dissecting complex metabolic integration provides direct genetic evidence for CodY activation by guanine nucleotides. J Bacteriol. 2011;193(20):5637–48. doi: 10.1128/JB.05510-11 21856856
15. Caldwell R, Sapolsky R, Weyler W, Maile RR, Causey SC, Ferrari E, Correlation between Bacillus subtilis scoC phenotype and gene expression determined using microarrays for transcriptome analysis. J Bacteriol. 2001;183(24):7329–40. 11717292
16. Dod B, Balassa G, Raulet E, Jeannoda V, Spore control (sco) mutations in Bacillus subtilis. II. Sporulation and the production of extracellular protease and α-amylase by scoC mutants. Molec Gen Genet. 1978;163:45–56.
17. Higerd TB, Hoch JA, Spizizen J, Hyperprotease-producing mutants of Bacillus subtilis. J Bacteriol. 1972;112(2):1026–8. 4628743
18. Kallio PT, Fagelson JE, Hoch JA, Strauch MA, The transition state regulator Hpr of Bacillus subtilis is a DNA-binding protein. J Biol Chem. 1991;266(20):13411–7. 1906467
19. Belitsky BR, Barbieri G, Albertini AM, Ferrari E, Strauch MA, Sonenshein AL, Interactive Regulation by the Bacillus subtilis Global Regulators CodY and ScoC. Mol Microbiol. 2015;97(4):698–716. doi: 10.1111/mmi.13056 25966844
20. Mangan S, Alon U, Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci USA. 2003;100(21):11980–5. 14530388
21. Alon U, Network motifs: theory and experimental approaches. Nat Rev Genet. 2007;8(6):450–61. 17510665
22. den Hengst CD, van Hijum SA, Geurts JM, Nauta A, Kok J, Kuipers OP, The Lactococcus lactis CodY regulon: identification of a conserved cis-regulatory element. J Biol Chem. 2005;280(40):34332–42. 16040604
23. Guedon E, Sperandio B, Pons N, Ehrlich SD, Renault P, Overall control of nitrogen metabolism in Lactococcus lactis by CodY, and possible models for CodY regulation in Firmicutes. Microbiology. 2005;151(Pt 12):3895–909. 16339935
24. Belitsky BR, Sonenshein AL, Genetic and biochemical analysis of CodY-binding sites in Bacillus subtilis. J Bacteriol. 2008;190(4):1224–36. 18083814
25. Belitsky BR, Sonenshein AL, Roadblock repression of transcription by Bacillus subtilis CodY. J Mol Biol. 2011;411(4):729–43. doi: 10.1016/j.jmb.2011.06.012 21699902
26. Belitsky BR, Sonenshein AL, CodY-mediated regulation of guanosine uptake in Bacillus subtilis. J Bacteriol. 2011;193(22):6276–87. doi: 10.1128/JB.05899-11 21926227
27. Slack FJ, Mueller JP, Sonenshein AL, Mutations that relieve nutritional repression of the Bacillus subtilis dipeptide permease operon. J Bacteriol. 1993;175(15):4605–14. 8335620
28. Villapakkam AC, Handke LD, Belitsky BR, Levdikov VM, Wilkinson AJ, Sonenshein AL, Genetic and biochemical analysis of the interaction of Bacillus subtilis CodY with branched-chain amino acids. J Bacteriol. 2009;191(22):6865–76. doi: 10.1128/JB.00818-09 19749041
29. Serror P, Sonenshein AL, CodY is required for nutritional repression of Bacillus subtilis genetic competence. J Bacteriol. 1996;178(20):5910–5. 8830686
30. Smits WK, Hoa TT, Hamoen LW, Kuipers OP, Dubnau D, Antirepression as a second mechanism of transcriptional activation by a minor groove binding protein. Mol Microbiol. 2007;64(2):368–81. 17493123
31. Koide A, Perego M, Hoch JA, ScoC regulates peptide transport and sporulation initiation in Bacillus subtilis. J Bacteriol. 1999;181(13):4114–7. 10383984
32. Dod B, Balassa G, Spore control (sco) mutations in Bacillus subtilis. III. Regulation of extracellular protease synthesis in the spore control mutations scoC. Molec Gen Genet. 1978;163:57–63.
33. Perego M, Hoch JA, Sequence analysis and regulation of the hpr locus, a regulatory gene for protease production and sporulation in Bacillus subtilis. J Bacteriol. 1988;170(6):2560–7. 3131303
34. Henner DJ, Ferrari E, Perego M, Hoch JA, Location of the targets of the hpr-97, sacU32(Hy), and sacQ36(Hy) mutations in upstream regions of the subtilisin promoter. J Bacteriol. 1988;170(1):296–300. 2447063
35. Ogura M, Matsuzawa A, Yoshikawa H, Tanaka T, Bacillus subtilis SalA (YbaL) negatively regulates expression of scoC, which encodes the repressor for the alkaline exoprotease gene, aprE. J Bacteriol. 2004;186(10):3056–64. 15126467
36. Toma S, Del Bue M, Pirola A, Grandi G, nprR1 and nprR2 regulatory regions for neutral protease expression in Bacillus subtilis. J Bacteriol. 1986;167(2):740–3. 3090022
37. Derouiche A, Shi L, Bidnenko V, Ventroux M, Pigonneau N, Franz-Wachtel M, et al. Bacillus subtilis SalA is a phosphorylation-dependent transcription regulator that represses scoC and activates the production of the exoprotease AprE. Mol Microbiol. 2015;97(6):1195–208. doi: 10.1111/mmi.13098 26094643
38. Zeigler DR, Pragai Z, Rodriguez S, Chevreux B, Muffler A, Albert T, et al. The origins of 168, W23, and other Bacillus subtilis legacy strains. J Bacteriol. 2008;190(21):6983–95. doi: 10.1128/JB.00722-08 18723616
39. Yanisch-Perron C, Vieira J, Messing J, Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–19. 2985470
40. Atkinson MR, Wray LV, Jr.Fisher SH, Regulation of histidine and proline degradation enzymes by amino acid availability in Bacillus subtilis. J Bacteriol. 1990;172(9):4758–65. 2118500
41. Sambrook J, Fritsch EF, Maniatis TJ, Molecular cloning: a laboratory manual, 2nd ed Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 1989.
42. Daniel RA, Haiech J, Denizot F, Errington J, Isolation and characterization of the lacA gene encoding beta-galactosidase in Bacillus subtilis and a regulator gene, lacR. J Bacteriol. 1997;179(17):5636–8. 9287030
43. Guerout-Fleury AM, Shazand K, Frandsen N, Stragier P, Antibiotic-resistance cassettes for Bacillus subtilis. Gene. 1995;167(1–2):335–6. 8566804
44. Mueller JP, Bukusoglu G, Sonenshein AL, Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: control of gsiA by the ComP-ComA signal transduction system. J Bacteriol. 1992;174(13):4361–73. 1378051
45. Berkmen MB, Lee CA, Loveday EK, Grossman AD, Polar positioning of a conjugation protein from the integrative and conjugative element ICEBs1 of Bacillus subtilis. J Bacteriol. 2010;192(1):38–45. doi: 10.1128/JB.00860-09 19734305
46. Belitsky BR, Sonenshein AL, Role and regulation of Bacillus subtilis glutamate dehydrogenase genes. J Bacteriol. 1998;180(23):6298–305. 9829940
47. Barbieri G, Voigt B, Albrecht D, Hecker M, Albertini AM, Sonenshein AL, et al. CodY regulates expression of the Bacillus subtilis extracellular proteases Vpr and Mpr. J Bacteriol. 2015;197:1423–32. doi: 10.1128/JB.02588-14 25666135
48. Chary VK, Amaya EI, Piggot PJ, Neomycin- and spectinomycin-resistance replacement vectors for Bacillus subtilis. FEMS Microbiol Lett. 1997;153(1):135–9. 9252583