DOI: 10.1128/jb.00128-09. Varying Rate of RNA Chain Elongation during <i>rrn</i> Transcription in <i>Escherichia coli</i>

Varying Rate of RNA Chain Elongation during rrn Transcription in Escherichia coli

10.1128/jb.00128-09

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

ABSTRACT The value of the rRNA chain elongation rate in bacteria is an important physiological parameter, as it affects not only the rRNA promoter activity but also the free-RNA polymerase concentration and thereby the transcription of all genes. On average, rRNA chains elongate at a rate of 80 to 90 nucleotides (nt) per s, and the transcription of an entire rrn operon takes about 60 s (at 37°C). Here we have analyzed a reported distribution obtained from electron micrographs of RNA polymerase molecules along rrn operons in E. coli growing at 2.5 doublings per hour (S. Quan, N. Zhang, S. French, and C. L. Squires, J. Bacteriol. 187:1632-1638, 2005). The distribution exhibits two peaks of higher polymerase density centered within the 16S and 23S rRNA genes. An evaluation of this distribution indicates that RNA polymerase transcribes the 5′ leader region at speeds up to or greater than 250 nt/s. Once past the leader, transcription slows down to about 65 nt/s within the 16S gene, speeds up in the spacer region between the 16S and 23S genes, slows again to about 65 nt/s in the 23S region, and finally speeds up to a rate greater than 400 nt/s near the end of the operon. We suggest that the slowing of transcript elongation in the 16S and 23S sections is the result of transcriptional pauses, possibly caused by temporary interactions of the RNA polymerase with secondary structures in the nascent rRNA.

Bibliography

Dennis, P. P., Ehrenberg, M., Fange, D., & Bremer, H. (2009). Varying Rate of RNA Chain Elongation during rrn Transcription in Escherichia coli. Journal of Bacteriology, 191(11), 3740â3746.

Authors 4

P. P. Dennis (first)
M. Ehrenberg (additional)
D. Fange (additional)
H. Bremer (additional)

References 23 Referenced 38

Albrechtsen, B., C. L. Squires, S. Li, and C. Squires. 1990. Antitermination of characterized transcription terminators by the Escherichia coli rrnG leader region. J. Mol. Biol. 213 : 123-134. (10.1016/S0022-2836(05)80125-1) / J. Mol. Biol. (1990)
Bai, L., A. Shundrovsky, and M. D. Wang. 2004. Sequence-dependent kinetic model of transcription elongation by RNA polymerase. J. Mol. Biol. 344 : 335-340. (10.1016/j.jmb.2004.08.107) / J. Mol. Biol. (2004)
Bai, L., T. J. Santangelo, and M. D. Wang. 2006. Single-molecule analysis of RNA polymerase transcription. Annu. Rev. Biophys. Biomol. Struct. 35 : 343-360. (10.1146/annurev.biophys.35.010406.150153) / Annu. Rev. Biophys. Biomol. Struct. (2006)
10.1128/JB.180.2.265-273.1998
Bremer, H., and L. Berry. 1971. Co-transcription of 16s and 23s r-RNA in E. coli. Nat. New Biol. 234 : 81-82. / Nat. New Biol. (1971)
EcoSal—Escherichia coli and Salmonella: cellular and molecular biology 2008
Bremer, H., P. P. Dennis, and M. Ehrenberg. 2003. Free RNA polymerase and modeling global transcription in Escherichia coli. Biochimie 85 : 597-609. (10.1016/S0300-9084(03)00105-6) / Biochimie (2003)
Condon, C., S. French, C. Squires, and C. L. Squires. 1993. Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies. EMBO J. 12 : 4305-4315. (10.1002/j.1460-2075.1993.tb06115.x) / EMBO J. (1993)
Dennis, P. P., and H. Bremer. 1973. Regulation of ribonucleic acid synthesis in Escherichia coli B/r: an analysis of a shift-up. I. Ribosomal RNA chain growth rates. J. Mol. Biol. 75 : 145-159. (10.1016/0022-2836(73)90535-4) / J. Mol. Biol. (1973)
10.1128/MMBR.68.4.639-668.2004
Epshtein, V., and E. Nudler. 2003. Cooperation between RNA polymerase molecules in transcription elongation. Science 300 : 801-805. (10.1126/science.1083219) / Science (2003)
Farnham, P. J., and T. Platt. 1981. Rho-independent termination: dyad symmetry in DNA causes RNA polymerase to pause during transcription in vitro. Nucleic Acids Res. 9 : 563-577. (10.1093/nar/9.3.563) / Nucleic Acids Res. (1981)
Gillespie, D. 1977. Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81 : 2340-2361. (10.1021/j100540a008) / J. Phys. Chem. (1977)
10.1128/jb.173.20.6647-6649.1991
Kingston, R. E., and M. Chamberlin. 1981. Pausing and attenuation of in vitro transcription in the rrnB operon of E. coli. Cell 27 : 523-531. (10.1016/0092-8674(81)90394-9) / Cell (1981)
Nudler, E., A. Mustaev, E. Lukhtanov, and A. Goldfarb. 1997. The RNA-DNA hybrid maintains the register of transcription by preventing backtracking of RNA polymerase. Cell 89 : 33-41. (10.1016/S0092-8674(00)80180-4) / Cell (1997)
10.1128/JB.187.5.1632-1638.2005
10.1128/jb.151.2.879-887.1982
10.1128/jb.176.10.2807-2813.1994
Vogel, U., and K. F. Jensen. 1995. Effects of the antiterminator BoxA on transcription elongation kinetics and ppGpp inhibition of transcription elongation in Escherichia coli. J. Biol. Chem. 270 : 18335-18340. (10.1074/jbc.270.31.18335) / J. Biol. Chem. (1995)
10.1128/JB.181.14.4170-4175.1999
Zellars, M., and C. L. Squires. 1999. Antiterminator-dependent modulation of transcription elongation rates by NusB and NusG. Mol. Microbiol. 32 : 1296-1304. (10.1046/j.1365-2958.1999.01442.x) / Mol. Microbiol. (1999)
Zhang, X., P. Dennis, M. Ehrenberg, and H. Bremer. 2002. Kinetic properties of rrn promoters in E. coli. Biochimie 84 : 981-996. (10.1016/S0300-9084(02)00010-X) / Biochimie (2002)

Dates

Type	When
Created	16 years, 5 months ago (March 30, 2009, 12:24 p.m.)
Deposited	4 years, 1 month ago (July 29, 2021, 1:45 p.m.)
Indexed	1 year ago (Aug. 26, 2024, 11:50 a.m.)
Issued	16 years, 3 months ago (June 1, 2009)
Published	16 years, 3 months ago (June 1, 2009)
Published Print	16 years, 3 months ago (June 1, 2009)

Funders 0

None

BibTeX

@article{Dennis_2009, title={Varying Rate of RNA Chain Elongation during rrn Transcription in Escherichia coli}, volume={191}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.00128-09}, DOI={10.1128/jb.00128-09}, number={11}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Dennis, P. P. and Ehrenberg, M. and Fange, D. and Bremer, H.}, year={2009}, month=jun, pages={3740–3746} }

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  "abstract": "<jats:title>ABSTRACT</jats:title>\n          <jats:p>\n            The value of the rRNA chain elongation rate in bacteria is an important physiological parameter, as it affects not only the rRNA promoter activity but also the free-RNA polymerase concentration and thereby the transcription of all genes. On average, rRNA chains elongate at a rate of 80 to 90 nucleotides (nt) per s, and the transcription of an entire\n            <jats:italic>rrn</jats:italic>\n            operon takes about 60 s (at 37\u00b0C). Here we have analyzed a reported distribution obtained from electron micrographs of RNA polymerase molecules along\n            <jats:italic>rrn</jats:italic>\n            operons in\n            <jats:italic>E. coli</jats:italic>\n            growing at 2.5 doublings per hour (S. Quan, N. Zhang, S. French, and C. L. Squires, J. Bacteriol. 187:1632-1638, 2005). The distribution exhibits two peaks of higher polymerase density centered within the 16S and 23S rRNA genes. An evaluation of this distribution indicates that RNA polymerase transcribes the 5\u2032 leader region at speeds up to or greater than 250 nt/s. Once past the leader, transcription slows down to about 65 nt/s within the 16S gene, speeds up in the spacer region between the 16S and 23S genes, slows again to about 65 nt/s in the 23S region, and finally speeds up to a rate greater than 400 nt/s near the end of the operon. We suggest that the slowing of transcript elongation in the 16S and 23S sections is the result of transcriptional pauses, possibly caused by temporary interactions of the RNA polymerase with secondary structures in the nascent rRNA.\n          </jats:p>",
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