GTP dysregulation in Bacillus subtilis cells lacking (p)ppGpp results in phenotypic amino acid auxotrophy and failure to adapt to nutrient downshift and regulate biosynthesis genes

Journal of Bacteriology

Volumn 196, Issue 1, 2014, Pages 189-201

  Kriel, Allison ^a,b   Brinsmade, Shaun R ^c   Tse, Jessica L ^d,e   Tehranchi, Ashley K ^b   Bittner, Alycia N ^d   Sonenshein, Abraham L ^c   Wang, Jue D ^a,b,d  

^a Department of Molecular and Human Genetics ^*  (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ARGININE; GUANOSINE; GUANOSINE TRIPHOSPHATE; HISTIDINE; ISOLEUCINE; LEUCINE; METHIONINE; THREONINE; TRANSCRIPTION FACTOR; TRYPTOPHAN; VALINE;

ADAPTATION; ARTICLE; AUXOTROPHY; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; BIOSYNTHESIS; COLONY FORMATION; CONTROLLED STUDY; GENE CONTROL; LOSS OF FUNCTION MUTATION; NONHUMAN; OPERON; POINT MUTATION; PRIORITY JOURNAL; STRESS;

ADAPTATION, PHYSIOLOGICAL; AMINO ACIDS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BIOSYNTHETIC PATHWAYS; GENE EXPRESSION REGULATION, BACTERIAL; GUANOSINE PENTAPHOSPHATE; GUANOSINE TETRAPHOSPHATE; GUANOSINE TRIPHOSPHATE; POINT MUTATION;

EID: 84890289940     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00918-13     Document Type: Article

References (44)

1. Potrykus K, Cashel M. 2008. (p) ppGpp: still magical? Annu. Rev. Microbiol. 62:35-51. http://dx.doi.org/10.1146/annurev.micro.62.081307.162903.
2. Xiao H, Kalman M, Ikehara K, Zemel S, Glaser G, Cashel M. 1991. Residual guanosine 3=,5=-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J. Biol. Chem. 266: 5980-5990.
3. Murphy H, Cashel M. 2003. Isolation of RNA polymerase suppressors of a (p)ppGpp deficiency. Methods Enzymol. 371:596-601. http://dx.doi.org/10.1016/S0076-6879(03)71044-1.
4. Paul BJ, Barker MM, Ross W, Schneider DA, Webb C, Foster JW, Gourse RL. 2004. DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP. Cell 118:311-322. http://dx.doi.org/10.1016/j.cell.2004.07.009.
5. Paul BJ, Berkmen MB, Gourse RL. 2005. DksA potentiates direct activation of amino acid promoters by ppGpp. Proc. Natl. Acad. Sci. U. S. A. 102:7823-7828. http://dx.doi.org/10.1073/pnas.0501170102.
6. Barker MM, Gaal T, Gourse RL. 2001. Mechanism of regulation of transcription initiation by ppGpp. II. Models for positive control based on properties of RNAP mutants and competition for RNAP. J. Mol. Biol. 305:689-702. http://dx.doi.org/10.1006/jmbi.2000.4328.
7. Haugen SP, Berkmen MB, Ross W, Gaal T, Ward C, Gourse RL. 2006. rRNA promoter regulation by nonoptimal binding of sigma region 1.2: an additional recognition element forRNApolymerase. Cell 125:1069-1082. http://dx.doi.org/10.1016/j.cell.2006.04.034.
8. Traxler MF, Summers SM, Nguyen HT, Zacharia VM, Hightower GA, Smith JT, Conway T. 2008. The global, ppGpp-mediated stringent response to amino acid starvation in Escherichia coli. Mol. Microbiol. 68: 1128-1148. http://dx.doi.org/10.1111/j.1365-2958.2008.06229.x.
9. Wendrich TM, Marahiel MA. 1997. Cloning and characterization of a relA/spoT homologue from Bacillus subtilis. Mol. Microbiol. 26:65-79. http://dx.doi.org/10.1046/j.1365-2958.1997.5511919.x.
10. Srivatsan A, Han Y, Peng J, Tehranchi AK, Gibbs R, Wang JD, Chen R. 2008. High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet. 4:e1000139. http://dx.doi.org/10.1371/journal.pgen.1000139.
11. Nanamiya H, Kasai K, Nozawa A, Yun CS, Narisawa T, Murakami K, Natori Y, Kawamura F, Tozawa Y. 2008. Identification and functional analysis of novel (p) ppGpp synthetase genes in Bacillus subtilis. Mol. Microbiol. 67:291-304. http://dx.doi.org/10.1111/j.1365-2958.2007.06018.x.
12. Kriel A, Bittner AN, Kim SH, Liu K, Tehranchi AK, Zou WY, Rendon S, Chen R, Tu BP, Wang JD. 2012. Direct regulation of GTP homeostasis by (p)ppGpp: a critical component of viability and stress resistance. Mol. Cell 48:231-241. http://dx.doi.org/10.1016/j.molcel.2012.08.009.
13. Brinsmade SR, Sonenshein AL. 2011. Dissecting complex metabolic integration provides direct genetic evidence for CodY activation by guanine nucleotides. J. Bacteriol. 193:5637-5648. http://dx.doi.org/10.1128/JB.05510-11.
14. Molle V, Nakaura Y, Shivers RP, Yamaguchi H, Losick R, Fujita Y, Sonenshein AL. 2003. Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome- wide transcript analysis. J. Bacteriol. 185:1911-1922. http://dx.doi.org/10.1128/JB.185.6.1911-1922.2003.
15. Tojo S, Satomura T, Morisaki K, Deutscher J, Hirooka K, Fujita Y. 2005. Elaborate transcription regulation of the Bacillus subtilis ilv-leu operon involved in the biosynthesis of branched-chain amino acids through global regulators of CcpA, CodY and TnrA. Mol. Microbiol. 56: 1560-1573. http://dx.doi.org/10.1111/j.1365-2958.2005.04635.x.
16. Belitsky BR, Sonenshein AL. 2013. Genome-wide identification of Bacillus subtilis CodY-binding sites at single-nucleotide resolution. Proc. Natl. Acad. Sci. U. S. A. 110:7026-7031. http://dx.doi.org/10.1073/pnas.1300428110.
17. Tojo S, Satomura T, Kumamoto K, Hirooka K, Fujita Y. 2008. Molecular mechanisms underlying the positive stringent response of the Bacillus subtilis ilv-leu operon, involved in the biosynthesis of branched-chain amino acids. J. Bacteriol. 190:6134-6147. http://dx.doi.org/10.1128/JB.00606-08.
18. Krasny L, Tiserova H, Jonak J, Rejman D, Sanderova H. 2008. The identity of the transcription -1 position is crucial for changes in gene expression in response to amino acid starvation in Bacillus subtilis. Mol. Microbiol. 69:42-54. http://dx.doi.org/10.1111/j.1365-2958.2008.06256.x.
19. Schaeffer P, Millet J, Aubert JP. 1965. Catabolic repression of bacterial sporulation. Proc. Natl. Acad. Sci. U. S. A. 54:704-711. http://dx.doi.org/10.1073/pnas.54.3.704.
20. Vasantha N, Freese E. 1980. Enzyme changes during Bacillus subtilis sporulation caused by deprivation of guanine nucleotides. J. Bacteriol. 144:1119-1125.
21. Spizizen J. 1958. Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc. Natl. Acad. Sci. U. S. A. 44: 1072-1078. http://dx.doi.org/10.1073/pnas.44.10.1072.
22. Harwood CR, Cutting SM. 1990. Molecular biological methods for Bacillus. John Wiley & Sons, Inc., New York, NY.
23. Janes BK, Stibitz S. 2006. Routine markerless gene replacement in Bacillus anthracis. Infect. Immun. 74:1949-1953. http://dx.doi.org/10.1128/IAI.74.3.1949-1953.2006.
24. Vagner V, Dervyn E, Ehrlich SD. 1998. A vector for systematic gene inactivation in Bacillus subtilis. Microbiology 144:3097-3104. http://dx.doi.org/10.1099/00221287-144-11-3097.
25. Brinsmade SR, Kleijn RJ, Sauer U, Sonenshein AL. 2010. Regulation of CodY activity through modulation of intracellular branched-chain amino acid pools. J. Bacteriol. 192:6357-6368. http://dx.doi.org/10.1128/JB.00937-10.
26. Wang JD, Sanders GM, Grossman AD. 2007. Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128:865-875. http://dx.doi.org/10.1016/j.cell.2006.12.043.
27. Britton RA, Eichenberger P, Gonzalez-Pastor JE, Fawcett P, Monson R, Losick R, Grossman AD. 2002. Genome-wide analysis of the stationaryphase sigma factor (sigma-H) regulon of Bacillus subtilis. J. Bacteriol. 184:4881-4890. http://dx.doi.org/10.1128/JB.184.17.4881-4890.2002.
28. Tusher VG, Tibshirani R, Chu G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 98:5116-5121. http://dx.doi.org/10.1073/pnas.091062498.
29. de Hoon MJ, Imoto S, Nolan J, Miyano S. 2004. Open source clustering software. Bioinformatics 20:1453-1454. http://dx.doi.org/10.1093/bioinformatics/bth078.
30. Eisen M.B Spellman PT, Brown PO, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95:14863-14868. http://dx.doi.org/10.1073/pnas.95.25.14863.
31. Saldanha AJ. 2004. Java Treeview-extensible visualization of microarray data. Bioinformatics 20:3246-3248. http://dx.doi.org/10.1093/bioinformatics/bth349.
32. Hogg T, Mechold U, Malke H, Cashel M, Hilgenfeld R. 2004. Conformational antagonism between opposing active sites in a bifunctional RelA/SpoT homolog modulates (p)ppGpp metabolism during the stringent response. Cell 117:57-68. (Erratum, 117:415.) http://dx.doi.org/10.1016/S0092-8674(04)00260-0.
33. Yeggy JP, Stahly DP. 1980. Sporulation and regulation of homoserine dehydrogenase in Bacillus subtilis. Can. J. Microbiol. 26:1386-1391. http://dx.doi.org/10.1139/m80-231.
34. Yasbin RE, Fields PI, Andersen BJ. 1980. Properties of Bacillus subtilis 168 derivatives freed of their natural prophages. Gene 12:155-159. http://dx.doi.org/10.1016/0378-1119(80)90026-8.
35. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, Arnaud M, Asai K, Ashikaga S, Aymerich S, Bessieres P, Boland F, Brignell SC, Bron S, Bunai K, Chapuis J, Christiansen LC, Danchin A, Debarbouille M, Dervyn E, Deuerling E, Devine K, Devine SK, Dreesen O, Errington J, Fillinger S, Foster SJ, Fujita Y, Galizzi A, Gardan R, Eschevins C, Fukushima T, Haga K, Harwood CR, Hecker M, Hosoya D, Hullo MF, Kakeshita H, Karamata D, Kasahara Y, Kawamura F, Koga K, Koski P, Kuwana R, Imamura D, Ishimaru M, Ishikawa S, Ishio I, Le Coq D, Masson A, Mauel C, Meima R, Mellado RP, et al. 2003. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. U. S. A. 100:4678-4683. http://dx.doi.org/10.1073/pnas.0730515100.
36. Ebbole DJ, Zalkin H. 1987. Cloning and characterization of a 12-gene cluster from Bacillus subtilis encoding nine enzymes for de novo purine nucleotide synthesis. J. Biol. Chem. 262:8274-8287.
37. Eymann C, Homuth G, Scharf C, Hecker M. 2002. Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis. J. Bacteriol. 184:2500-2520. http://dx.doi.org/10.1128/JB.184.9.2500-2520.2002.
38. Handke LD, Shivers RP, Sonenshein AL. 2008. Interaction of Bacillus subtilis CodY with GTP. J. Bacteriol. 190:798-806. http://dx.doi.org/10.1128/JB.01115-07.
39. Ratnayake-Lecamwasam M, Serror P, Wong KW, Sonenshein AL. 2001. Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev. 15:1093-1103. http://dx.doi.org/10.1101/gad.874201.
40. Krasny L, Gourse RL. 2004. An alternative strategy for bacterial ribosome synthesis: Bacillus subtilis rRNA transcription regulation. EMBO J. 23: 4473-4483. http://dx.doi.org/10.1038/sj.emboj.7600423.
41. Tojo S, Kumamoto K, Hirooka K, Fujita Y. 2010. Heavy involvement of stringent transcription control depending on the adenine or guanine species of the transcription initiation site in glucose and pyruvate metabolism in Bacillus subtilis. J. Bacteriol. 192:1573-1585. http://dx.doi.org/10.1128/JB.01394-09.
42. Helmann JD. 1995. Compilation and analysis of Bacillus subtilis sigma A-dependent promoter sequences: evidence for extended contact between RNA polymerase and upstream promoter DNA. Nucleic Acids Res. 23: 2351-2360. http://dx.doi.org/10.1093/nar/23.13.2351.
43. Tehranchi AK, Blankschien MD, Zhang Y, Halliday JA, Srivatsan A, Peng J, Herman C, Wang JD. 2010. The transcription factor DksA prevents conflicts between DNA replication and transcription machinery. Cell 141:595-605. http://dx.doi.org/10.1016/j.cell.2010.03.036.
44. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese- Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH. 2011. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39:D225-D229. http://dx.doi.org/10.1093/nar/gkq1189.