The Bacillus subtilis tyrZ gene encodes a highly selective tyrosyl tRNA synthetase and is regulated by a MarR regulator and T box riboswitch

Journal of Bacteriology

Volumn 197, Issue 9, 2015, Pages 1624-1631

  Williams Wagner, Rebecca N ^a   Grundy, Frank J ^a   Raina, Medha ^a,b   Ibba, Michael ^a   Henkin, Tina M ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALANINE; AMINO ACID; MULTIPLE ANTIBIOTIC RESISTANCE REPRESSOR PROTEIN; NEOMYCIN; NUCLEOTIDE; REPRESSOR PROTEIN; T BOX TRANSCRIPTION FACTOR; THREONINE; TYROSINE; TYROSINE TRANSFER RNA LIGASE; UNCLASSIFIED DRUG; RIBOSWITCH; TRANSCRIPTION FACTOR;

AMINOACYLATION; ANTIBIOTIC RESISTANCE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM COLONY; BACTERIUM ISOLATION; BIOFILM; CELL GROWTH; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIMERIZATION; ENZYME REGULATION; GENE ACTIVATION; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE INACTIVATION; GENE INSERTION; GENE MUTATION; GENE REPRESSION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC CODE; GENETIC SELECTION; GENETIC TRANSCRIPTION; GROWTH INHIBITION; GROWTH RATE; IN VITRO STUDY; INCUBATION TIME; NONHUMAN; OPERATOR GENE; PREDICTION; PRIORITY JOURNAL; PROMOTER REGION; RIBOSWITCH; SOLUBILITY; START CODON; STOP CODON; TRANSLATION INITIATION; TYRS GENE; TYRZ GENE; ENZYME SPECIFICITY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

BACILLUS SUBTILIS;

BACILLUS SUBTILIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; RIBOSWITCH; SUBSTRATE SPECIFICITY; TRANSCRIPTION FACTORS; TYROSINE; TYROSINE-TRNA LIGASE;

EID: 84928403908     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00008-15     Document Type: Article

References (43)

1. Ling J, Reynolds N, Ibba M. 2009. Aminoacyl-tRNA synthesis and translational quality control. Annu Rev Microbiol 63:61-78. http://dx.doi.org/10.1146/annurev.micro.091208.073210.
2. Calendar R, Berg P. 1967. D-Tyrosyl RNA: formation, hydrolysis and utilization for protein synthesis. J Mol Biol 26:39-54. http://dx.doi.org/10.1016/0022-2836(67)90259-8.
3. Leiman SA, May JM, Lebar MD, Kahne D, Kolter R, Losick R. 2013. D-Amino acids indirectly inhibit biofilm formation in Bacillus subtilis by interfering with protein synthesis. J Bacteriol 195:5391-5395. http://dx.doi.org/10.1128/JB.00975-13.
4. Leiman SA, Richardson C, Foulston L, Elsholz AKW, First EA, Losick R. 2015. Identification and characterization of mutations conferring resistance to D-amino acids in Bacillus subtilis. J Bacteriol 197:1632-1639. http://dx.doi.org/10.1128/JB.00009-15.
5. Champney WS, Jensen RA. 1970. The enzymology of prephenate dehydrogenase in Bacillus subtilis. J Biol Chem 245:3763-3770.
6. Champney WS, Jensen RA. 1969. D-Tyrosine as a metabolic inhibitor of Bacillus subtilis. J Bacteriol 98:205-214.
7. Lam H, Oh D, Cava F, Takacs CN, Clardy J, de Pedro MA, Waldor MK. 2009. D-Amino acids govern stationary phase cell wall remodeling in bacteria. Science 325:1552-1555. http://dx.doi.org/10.1126/science.1178123.
8. Stein T. 2005. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845-857. http://dx.doi.org/10.1111/j.1365-2958.2005.04587.x.
9. Soutourina J, Blanquet S, Plateau P. 2000. D-Tyrosyl-tRNATyr metabolism in Saccharomyces cerevisiae. J Biol Chem 275:11626-11630. http://dx.doi.org/10.1074/jbc.275.16.11626.
10. Soutourina O, Soutourina J, Blanquet S, Plateau P. 2004. Formation of D-tyrosyl-tRNATyr accounts for the toxicity of D-tyrosine toward Escherichia coli. J Biol Chem 279:42560-42565. http://dx.doi.org/10.1074/jbc.M402931200.
11. Glaser PA, Kunst F, Debarbouille M, Vertes A, Danchin A, Dedonder R. 1991. A gene encoding a tyrosine tRNA synthetase is located near sacS in Bacillus subtilis. DNA Seq 1:251-261.
12. Henkin TM, Glass BL, Grundy FJ. 1992. Analysis of the Bacillus subtilis tyrS gene: conservation of a regulatory sequence in multiple tRNA synthetase genes. J Bacteriol 174:1299-1306.
13. Sulavik MC, Gambino LF, Miller PF. 1995. The MarR repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli: prototypic member of a family of bacterial regulatory proteins involved in sensing phenolic compounds. Mol Med 1:436-446.
14. Rocha ER, Herren CD, Smalley DJ, Smith CJ. 2003. The complex oxidative stress response of Bacteroides fragilis: the role of OxyR in control of gene expression. Anaerobe 9:165-173. http://dx.doi.org/10.1016/S1075-9964(03)00118-5.
15. Kim J, Inaoka T, Hirooka K, Matsuoka H, Murata M, Ohki R, Adachi Y, Fujita Y, Ochi K. 2009. Identification and characterization of a novel multidrug resistance operon, mdtRP (yusOP), of Bacillus subtilis. J Bacteriol 191:3273-3281. http://dx.doi.org/10.1128/JB.00151-09.
16. Escudero JA, Millan AS, Montero N, Gutierrez B, Ovejero CM, Carrilero L, González-Zorn B. 2013. SatR is a repressor of fluoroquinolone efflux pump SatAB. Antimicrob Agents Chemother 57:3430-3433. http://dx.doi.org/10.1128/AAC.00515-13.
17. Teixeira FL, dos Santos Silva DN, Pauer H, Ferreira LQ, Ferreira E, Domingues RMCP, Lobo LA. 2013. The role of BmoR, a MarR family regulator, in the survival of Bacteroides fragilis during oxidative stress. Int J Med Micriobiol 303:443-448. http://dx.doi.org/10.1016/j.ijmm.2013.05.007.
18. Martin RG, Rosner JL. 1995. Binding of purified multiple antibioticresistance repressor protein (MarR) to mar operator sequences. Proc Natl Acad SciUSA92:5456-5460. http://dx.doi.org/10.1073/pnas.92.12.5456.
19. Wilkinson SP, Grove A. 2004. HucR, a novel uric acid-responsive member of the MarR family of transcriptional regulators from Deinococcus radiodurans. J Biol Chem 279:51442-51450. http://dx.doi.org/10.1074/jbc.M405586200.
20. Perera IC, Grove A. 2010. Molecular mechanisms of ligand-mediated attenuation of DNA binding by MarR family transcriptional regulators. J Mol Cell Biol 2:243-254. http://dx.doi.org/10.1093/jmcb/mjq021.
21. Grundy FJ, Henkin TM. 1993. tRNA as a positive regulator of transcription antitermination in B. subtilis. Cell 74:475-482. http://dx.doi.org/10.1016/0092-8674(93)80049-K.
22. Grundy FJ, Rollins SM, Henkin TM. 1994. Interaction between the acceptor end of tRNA and the T box stimulates antitermination in the Bacillus subtilis tyrS gene: a new role for the discriminator base. J Bacteriol 176:4518-4526.
23. Yousef MR, Grundy FJ, Henkin TM. 2003. tRNA requirements for glyQS antitermination: a new twist on tRNA. RNA 9:1148-1156. http://dx.doi.org/10.1261/rna.5540203.
24. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
25. Anagnostopoulos C, Spizizen J. 1961. Requirements for transformation in Bacillus subtilis. J Bacteriol 81:741-746.
26. Branda SS, González-Pastor JE, Ben-Yehuda S, Losick R, Kolter R. 2001. Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci U S A 98:11621-11626. http://dx.doi.org/10.1073/pnas.191384198.
27. Zuber P, Losick R. 1987. Role of AbrB in Spo0A-and Spo0B-dependent utilization of a sporulation promoter in Bacillus subtilis. J Bacteriol 169:2223-2230.
28. Nakano MM, Zuber P. 1989. Cloning and characterization of srfB, a regulatory gene involved in surfactin production and competence in Bacillus subtilis. J Bacteriol 171:5347-5353.
29. Itaya M, Kondo K, Tanaka T. 1989. A neomycin resistance gene cassette selectable in a single copy state in the Bacillus subtilis chromosome. Nucleic Acids Res 17:4410. http://dx.doi.org/10.1093/nar/17.11.4410.
30. Grundy FJ, Henkin TM. 1998. The S box regulon: a new global transcription termination control system for methionine and cysteine biosynthesis genes in gram-positive bacteria. Mol Microbiol 30:737-749. http://dx.doi.org/10.1046/j.1365-2958.1998.01105.x.
31. Yasbin RE, Young FE. 1974. Transduction in Bacillus subtilis by bacteriophage SPP1. J Virol 14:1343-1348.
32. Winkler WC. 2002. Ph.D. thesis. The Ohio State University, Columbus, OH.
33. Branda SS, Gonza E, Dervyn E, Ehrlich SD, Losick R, Kolter R. 2004. Genes involved in formation of structured multicellular communities by Bacillus subtilis. J Bacteriol 186:3970-3979. http://dx.doi.org/10.1128/JB.186.12.3970-3979.2004.
34. Woese CR, Olsen GJ, Ibba M, Söll D. 2000. Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol Mol Biol Rev 64:202-236. http://dx.doi.org/10.1128/MMBR.64.1.202-236.2000.
35. Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R, Losick R. 2010. D-Amino acids trigger biofilm disassembly. Science 328:627-629. http://dx.doi.org/10.1126/science.1188628.
36. Cava F, Lam H, de Pedro MA, Waldor MK. 2011. Emerging knowledge of regulatory roles of D-amino acids in bacteria. Cell Mol Life Sci 68:817-831. http://dx.doi.org/10.1007/s00018-010-0571-8.
37. Aronson JN, Wermus GR. 1965. Effects of m-tyrosine on growth and sporulation of Bacillus species. J Bacteriol 90:38-46.
38. Tempest DW, Meers JL, Brown CW. 1970. Influence of environment on the content and composition of microbial free amino acid pools. J Gen Microbiol 64:171-185. http://dx.doi.org/10.1099/00221287-64-2-171.
39. Hao Z, Lou H, Zhu R, Zhu J, Zhang D, Zhao BS, Zeng S, Chen X, Chan J, He C, Chen PR. 2014. The multiple antibiotic resistance regulator MarR is a copper sensor in Escherichia coli. Nat Chem Biol 10:21-28. http://dx.doi.org/10.1038/nchembio.1380.
40. Asai K, Yamaguchi H, Kang C, Yoshida K, Fujita Y, Sadaie Y. 2003. DNAmicroarray analysis of Bacillus subtilis sigma factors of extracytoplasmic function family. FEMS Microbiol Lett 220:155-160. http://dx.doi.org/10.1016/S0378-1097(03)00093-4.
41. Cao M, Salzberg L, Tsai CS, Masher T, Bonilla C, Wang T, Ye RW, Márquez-Magaña L, Helmann JD. 2003. Regulation of the Bacillus subtilis extracytoplasmic function protein _Y and its target promoters. J Bacteriol 185:4883-4890. http://dx.doi.org/10.1128/JB.185.16.4883-4890.2003.
42. 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.
43. Schneider TD, Stephens RM. 1990. Sequence Logos: a new way to displace consensus sequences. Nucleic Acids Res 18:6097-6100. http://dx.doi.org/10.1093/nar/18.20.6097.