A Stop Codon-dependent Internal Secondary Translation Initiation Region in Escherichia Coli RpoS

Overview

Journal RNA

Specialty Molecular Biology

Date 2004 Aug 20

PMID 15317973

Citations 6

Authors

Pochi Ramalingam Subbarayan

Malancha Sarkar

Affiliations

Soon will be listed here.

Abstract

Sigma S (sigmaS) encoded by rpoS is a stationary phase-specific sigma subunit of the Escherichia coli RNA polymerase holoenzyme. In many E. coli strains, rpoS has an amber stop as codon 33 (rpoSAm), resulting in a 32-amino-acid-long peptide. Nevertheless, suppressor-free rpoSAm strains have functional sigmaS. This led us to hypothesize the presence of an intracistronic secondary translational initiation region (STIR) in the E. coli rpoS gene. Here, we demonstrate that the STIR is functional and is controlled by the upstream amber stop codon 33. Removal of the primary translational initiation region did not abolish translation from STIR, ruling out translational coupling. Importantly, the functional STIR conferred survival advantage. Taken together, our results reveal a hitherto unknown physiologically significant post-transcriptional process in E. coli rpoSAm strains.

Citing Articles

Genes within Genes in Bacterial Genomes.

Meydan S, Vazquez-Laslop N, Mankin A Microbiol Spectr. 2018; 6(4).

PMID: 30003865 PMC: 11633611. DOI: 10.1128/microbiolspec.RWR-0020-2018.

Comparative Proteomics Enables Identification of Nonannotated Cold Shock Proteins in E. coli.

DLima N, Khitun A, Rosenbloom A, Yuan P, Gassaway B, Barber K J Proteome Res. 2017; 16(10):3722-3731.

PMID: 28861998 PMC: 5647875. DOI: 10.1021/acs.jproteome.7b00419.

Expression and purification of recombinant Saccharomyces cerevisiae mitochondrial carrier protein YGR257Cp (Mtm1p).

Whittaker M, Whittaker J Protein Expr Purif. 2013; 93:77-86.

PMID: 24184947 PMC: 3876937. DOI: 10.1016/j.pep.2013.10.014.

Additional pathway to translate the downstream ndhK cistron in partially overlapping ndhC-ndhK mRNAs in chloroplasts.

Yukawa M, Sugiura M Proc Natl Acad Sci U S A. 2013; 110(14):5701-6.

PMID: 23509265 PMC: 3619338. DOI: 10.1073/pnas.1219914110.

The constancy of global regulation across a species: the concentrations of ppGpp and RpoS are strain-specific in Escherichia coli.

Ferenci T, Galbiati H, Betteridge T, Phan K, Spira B BMC Microbiol. 2011; 11:62.

PMID: 21439067 PMC: 3074542. DOI: 10.1186/1471-2180-11-62.

References

Subbarayan P, Sarkar M . Escherichia coli rpoS gene has an internal secondary translation initiation region. Biochem Biophys Res Commun. 2003; 313(2):294-9. DOI: 10.1016/j.bbrc.2003.11.132. View

Zambrano M, Kolter R . GASPing for life in stationary phase. Cell. 1996; 86(2):181-4. DOI: 10.1016/s0092-8674(00)80089-6. View

Shine J, Dalgarno L . Determinant of cistron specificity in bacterial ribosomes. Nature. 1975; 254(5495):34-8. DOI: 10.1038/254034a0. View

Smith R, PARKINSON J . Overlapping genes at the cheA locus of Escherichia coli. Proc Natl Acad Sci U S A. 1980; 77(9):5370-4. PMC: 350060. DOI: 10.1073/pnas.77.9.5370. View

Parker J . Errors and alternatives in reading the universal genetic code. Microbiol Rev. 1989; 53(3):273-98. PMC: 372737. DOI: 10.1128/mr.53.3.273-298.1989. View

Mulvey M, Loewen P . Nucleotide sequence of katF of Escherichia coli suggests KatF protein is a novel sigma transcription factor. Nucleic Acids Res. 1989; 17(23):9979-91. PMC: 335226. DOI: 10.1093/nar/17.23.9979. View

Lange R . Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol. 1991; 5(1):49-59. DOI: 10.1111/j.1365-2958.1991.tb01825.x. View

Cornelis S, Bruynooghe Y, Denecker G, Van Huffel S, Tinton S, Beyaert R . Identification and characterization of a novel cell cycle-regulated internal ribosome entry site. Mol Cell. 2000; 5(4):597-605. DOI: 10.1016/s1097-2765(00)80239-7. View

Inokuchi Y, Hirashima A, Sekine Y, Janosi L, Kaji A . Role of ribosome recycling factor (RRF) in translational coupling. EMBO J. 2000; 19(14):3788-98. PMC: 313962. DOI: 10.1093/emboj/19.14.3788. View

10.

Mukhopadhyay S, Audia J, Roy R, Schellhorn H . Transcriptional induction of the conserved alternative sigma factor RpoS in Escherichia coli is dependent on BarA, a probable two-component regulator. Mol Microbiol. 2000; 37(2):371-81. DOI: 10.1046/j.1365-2958.2000.01999.x. View

11.

Ishihama A . Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol. 2000; 54:499-518. DOI: 10.1146/annurev.micro.54.1.499. View

12.

Shultzaberger R, Bucheimer R, Rudd K, Schneider T . Anatomy of Escherichia coli ribosome binding sites. J Mol Biol. 2001; 313(1):215-28. DOI: 10.1006/jmbi.2001.5040. View

13.

Subbarayan P, Deutscher M . Escherichia coli RNase M is a multiply altered form of RNase I. RNA. 2002; 7(12):1702-7. PMC: 1370210. View

14.

Atlung T, Nielsen H, Hansen F . Characterisation of the allelic variation in the rpoS gene in thirteen K12 and six other non-pathogenic Escherichia coli strains. Mol Genet Genomics. 2002; 266(5):873-81. DOI: 10.1007/s00438-001-0610-0. View

15.

Jishage M, Kvint K, Shingler V, Nystrom T . Regulation of sigma factor competition by the alarmone ppGpp. Genes Dev. 2002; 16(10):1260-70. PMC: 186289. DOI: 10.1101/gad.227902. View

16.

Rajkumari K, Gowrishankar J . An N-terminally truncated RpoS (sigma(S)) protein in Escherichia coli is active in vivo and exhibits normal environmental regulation even in the absence of rpoS transcriptional and translational control signals. J Bacteriol. 2002; 184(12):3167-75. PMC: 135099. DOI: 10.1128/JB.184.12.3167-3175.2002. View

17.

Laursen B, de A Steffensen S, Hedegaard J, Moreno J, Mortensen K, Sperling-Petersen H . Structural requirements of the mRNA for intracistronic translation initiation of the enterobacterial infB gene. Genes Cells. 2002; 7(9):901-10. DOI: 10.1046/j.1365-2443.2002.00571.x. View

18.

Gowrishankar J, Yamamoto K, Subbarayan P, Ishihama A . In vitro properties of RpoS (sigma(S)) mutants of Escherichia coli with postulated N-terminal subregion 1.1 or C-terminal region 4 deleted. J Bacteriol. 2003; 185(8):2673-9. PMC: 152630. DOI: 10.1128/JB.185.8.2673-2679.2003. View

19.

Nyengaard N, Mortensen K, Lassen S, Hershey J . Tandem translation of E. coli initiation factor IF2 beta: purification and characterization in vitro of two active forms. Biochem Biophys Res Commun. 1991; 181(3):1572-9. DOI: 10.1016/0006-291x(91)92118-4. View

20.

Zambrano M, Siegele D, Almiron M, Tormo A, Kolter R . Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science. 1993; 259(5102):1757-60. DOI: 10.1126/science.7681219. View