Translation of TrpG in Bacillus Subtilis is Regulated by the Trp RNA-binding Attenuation Protein (TRAP)

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 1995 Aug 1

PMID 7543470

Citations 31

Authors

M Yang

A de Saizieu

A P van Loon

P Gollnick

Affiliations

Soon will be listed here.

Abstract

trpG of Bacillus subtilis encodes a glutamine amidotransferase subunit that is involved in the synthesis of both folic acid and L-tryptophan. Expression of trpG is negatively regulated by tryptophan even though this gene is located within a folic acid biosynthetic operon. Examination of both transcriptional and translational gene fusions to lacZ involving trpG and direct measurements of trpG mRNA levels and TrpG polypeptide accumulation demonstrated that translation of trpG is regulated by tryptophan whereas transcription is not. these studies also show that this regulation is mediated by the trp RNA-binding attenuation protein. Deletion and point mutations indicated that regulation is dependent on a series of G/UAG trinucleotide repeats surrounding the putative ribosome-binding site for trpG. Our results are consistent with a model in which the tryptophan-activated trp RNA-binding attenuation protein and ribosomes compete for binding to trpG mRNA.

Citing Articles

Solution structure, dynamics and tetrahedral assembly of Anti-TRAP, a homo-trimeric triskelion-shaped regulator of tryptophan biosynthesis in .

McElroy C, Ihms E, Yadav D, Holmquist M, Wadhwa V, Wysocki V J Struct Biol X. 2024; 10:100103.

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Posttranscription Initiation Control of Gene Expression Mediated by Bacterial RNA-Binding Proteins.

Babitzke P, Lai Y, Renda A, Romeo T Annu Rev Microbiol. 2019; 73:43-67.

PMID: 31100987 PMC: 9404307. DOI: 10.1146/annurev-micro-020518-115907.

RNA-binding proteins involved in post-transcriptional regulation in bacteria.

Van Assche E, Van Puyvelde S, Vanderleyden J, Steenackers H Front Microbiol. 2015; 6:141.

PMID: 25784899 PMC: 4347634. DOI: 10.3389/fmicb.2015.00141.

The Bacillus subtilis TRAP protein can induce transcription termination in the leader region of the tryptophan biosynthetic (trp) operon independent of the trp attenuator RNA.

McAdams N, Gollnick P PLoS One. 2014; 9(2):e88097.

PMID: 24505391 PMC: 3913778. DOI: 10.1371/journal.pone.0088097.

TRAP binding to the Bacillus subtilis trp leader region RNA causes efficient transcription termination at a weak intrinsic terminator.

Potter K, Merlino N, Jacobs T, Gollnick P Nucleic Acids Res. 2010; 39(6):2092-102.

PMID: 21097886 PMC: 3064811. DOI: 10.1093/nar/gkq965.

References

Babitzke P, Stults J, Shire S, Yanofsky C . TRAP, the trp RNA-binding attenuation protein of Bacillus subtilis, is a multisubunit complex that appears to recognize G/UAG repeats in the trpEDCFBA and trpG transcripts. J Biol Chem. 1994; 269(24):16597-604. View

Anagnostopoulos C, Spizizen J . REQUIREMENTS FOR TRANSFORMATION IN BACILLUS SUBTILIS. J Bacteriol. 1961; 81(5):741-6. PMC: 279084. DOI: 10.1128/jb.81.5.741-746.1961. View

KANE J . Regulation of a common amidotransferase subunit. J Bacteriol. 1977; 132(2):419-25. PMC: 221880. DOI: 10.1128/jb.132.2.419-425.1977. View

Hoch S, Roth C, Crawford I, Nester E . Control of tryptophan biosynthesis by the methyltryptophan resistance gene in Bacillus subtilis. J Bacteriol. 1971; 105(1):38-45. PMC: 248319. DOI: 10.1128/jb.105.1.38-45.1971. View

Henner D . Inducible expression of regulatory genes in Bacillus subtilis. Methods Enzymol. 1990; 185:223-8. DOI: 10.1016/0076-6879(90)85022-g. View

Gollnick P . Regulation of the Bacillus subtilis trp operon by an RNA-binding protein. Mol Microbiol. 1994; 11(6):991-7. DOI: 10.1111/j.1365-2958.1994.tb00377.x. View

Yansura D, Henner D . Use of the Escherichia coli lac repressor and operator to control gene expression in Bacillus subtilis. Proc Natl Acad Sci U S A. 1984; 81(2):439-43. PMC: 344692. DOI: 10.1073/pnas.81.2.439. View

Vogel H, Bonner D . Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956; 218(1):97-106. View

Simons R, Houman F, Kleckner N . Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987; 53(1):85-96. DOI: 10.1016/0378-1119(87)90095-3. View

10.

Antson A, Otridge J, Brzozowski A, Dodson E, Dodson G, Wilson K . The structure of trp RNA-binding attenuation protein. Nature. 1995; 374(6524):693-700. DOI: 10.1038/374693a0. View

11.

Cohen S, Chang A, Hsu L . Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A. 1972; 69(8):2110-4. PMC: 426879. DOI: 10.1073/pnas.69.8.2110. View

12.

Kuroda M, Shimotsu H, Henner D, Yanofsky C . Regulatory elements common to the Bacillus pumilus and Bacillus subtilis trp operons. J Bacteriol. 1986; 167(3):792-8. PMC: 215943. DOI: 10.1128/jb.167.3.792-798.1986. View

13.

Kuroda M, Henner D, Yanofsky C . cis-acting sites in the transcript of the Bacillus subtilis trp operon regulate expression of the operon. J Bacteriol. 1988; 170(7):3080-8. PMC: 211252. DOI: 10.1128/jb.170.7.3080-3088.1988. View

14.

KANE J, Holmes W, Jensen R . Metabolic interlock. The dual function of a folate pathway gene as an extra-operonic gene of tryptophan biosynthesis. J Biol Chem. 1972; 247(5):1587-96. View

15.

Slock J, Stahly D, Han C, Six E, Crawford I . An apparent Bacillus subtilis folic acid biosynthetic operon containing pab, an amphibolic trpG gene, a third gene required for synthesis of para-aminobenzoic acid, and the dihydropteroate synthase gene. J Bacteriol. 1990; 172(12):7211-26. PMC: 210846. DOI: 10.1128/jb.172.12.7211-7226.1990. View

16.

Henner D, Band L, Shimotsu H . Nucleotide sequence of the Bacillus subtilis tryptophan operon. Gene. 1985; 34(2-3):169-77. DOI: 10.1016/0378-1119(85)90125-8. View

17.

Melton D, Krieg P, Rebagliati M, Maniatis T, Zinn K, Green M . Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984; 12(18):7035-56. PMC: 320141. DOI: 10.1093/nar/12.18.7035. View

18.

Shimotsu H, Henner D . Construction of a single-copy integration vector and its use in analysis of regulation of the trp operon of Bacillus subtilis. Gene. 1986; 43(1-2):85-94. DOI: 10.1016/0378-1119(86)90011-9. View

19.

Shimotsu H, Kuroda M, Yanofsky C, Henner D . Novel form of transcription attenuation regulates expression the Bacillus subtilis tryptophan operon. J Bacteriol. 1986; 166(2):461-71. PMC: 214627. DOI: 10.1128/jb.166.2.461-471.1986. View

20.

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. DOI: 10.1016/0378-1119(85)90120-9. View