Growth-rate-dependent regulation of ribosome synthesis in E. coli: Expression of the lacZ and galK genes fused to ribosomal promoters

Miura, Akiko; Krueger, J H; Itoh, Seiga; Boer, H. H.; Nomura, Masayasu

doi:10.1016/0092-8674(81)90185-9

Cited by 97 publications

(57 citation statements)

References 43 publications

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“…With the exceptions of thrU, rplS and rpsMK the discriminator sequences of all promoters in this class differ in no more than one position from the corresponding consensus sequence. Only one other sequenced promoter, dnaA P., has a comparable fit to the r-protein consensus (22). This would be consistent with the observation that the dnaA product participates in the initiation of chromosomal replication (23), a step known to be blocked by aminoacid limitation (24,25).…”

Section: Consensus -A T T T T T C T -supporting

confidence: 83%

“…Thus the rate of expression of the rrnA P1 promoter is approximately proportional to the square of the growth rate (19) while those of the leuV and tyrT promoters are directly proportional (20,21). By contrast expression of the rpsE and rpsMR promoters is independent of growth rate, variation in the levels of the cognate mRNA species being achieved possibly by post transcriptional controls (22). A reciprocal class of promoters contains those which are required to be expressed efficiently on aminoacid limitation i.e.…”

Section: Consensus -A T T T T T C T -mentioning

confidence: 99%

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Conserved features of coordinately regulatedE.colipromoters

1984

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Section: Consensus -A T T T T T C T -supporting

confidence: 83%

Section: Consensus -A T T T T T C T -mentioning

confidence: 99%

Conserved features of coordinately regulatedE.colipromoters

1984

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“…The patterns forfrdABCD and narGHJI operon expression are similar to cat gene expression (20) but inverse to the pattern seen for control of rRNA and protein synthesis in response to growth rate (5,14,21,29).…”

Section: Resultsmentioning

confidence: 78%

Effect of cell growth rate on expression of the anaerobic respiratory pathway operons frdABCD, dmsABC, and narGHJI of Escherichia coli

et al. 1994

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The fumarate reductase (frdABCD), dimethyl sulfoxide (DMSO)-trimethylamine-N-oxide (TMAO) reductase (dmsABC), and nitrate reductase (narGHJI) operons in Escherichia coli encode enzymes involved in anaerobic respiration to the electron acceptors fumarate, DMSO or TMAO, and nitrate, respectively. They are regulated in response to anaerobiosis and nitrate availability. To determine how each operon is regulated in response to changes in cell growth rate and in oxygen availability, expression offrdA-lacZ, dmnsA-lacZ, and narG-lacZ fusion genes was examined during continuous culture. After a change in the cell growth rate, each anaerobic electron transport pathway operon fusion responded somewhat differently. WhereasfrdA-lacZ expression increased by fivefold as the growth rate decreased from 0.60 to 0.12/hour during aerobic growth, little change was seen under anaerobic conditions. In contrast, growth rate-dependent expression of narG-lacZ expression occurred under anaerobic conditions but not under aerobic conditions. Finally, dmsA-lacZ expression did not vary greatly for any of the growth rates tested. When cells were shifted from aerobic to anaerobic growth conditions, expression of each fusion increased at a moderate rate and peaked or "overshot" before reaching a new equilibrium value. This "overshoot" phenomenon was independent of the frr gene product, which functions as a transcriptional activator of each respiratory operon during anaerobic conditions. In contrast to the moderate rate of anaerobic induction seen for narG-lacZ expression, the addition of nitrate caused a rapid induction response. The cell appears to have many ways to adjust cell respiration in response to changes in cell growth conditions. Escherichia coli can respire either aerobically or anaerobically by using one of the alternative electron acceptors: oxygen, nitrate, trimethylamine-N-oxide (TMAO), dimethyl sulfoxide (DMSO), and fumarate. Depending on the availability of these respiratory substrates, the cell synthesizes one or more of the terminal enzymes of the electron transport pathways. DMSO-TMAO reductase, encoded by dmsABC, exhibits a broad substrate specificity for reducing TMAO, DMSO, and other amine-N-oxides (4, 28). Fumarate reductase readily catalyzes the interconversion of fumarate and succinate, although under physiological conditions, it is thought to perform the reductive reaction primarily during anaerobic growth (1). The four enzyme subunits are encoded by the frdABCD genes. The inducible nitrate reductase enzyme complex of E. coli which converts nitrate to nitrite during anaerobic cell growth is encoded by the narGHJI genes (13,27). The frdABCD, dmsABC, and narGHJI operons that encode the subunits of each enzyme complex are unlinked to one another and map at 94, 20, and 27 min on the E. coli chromosome, respectively (2).Expression of the anaerobic electron transport pathway operons is regulated in response to anaerobiosis and by the availability of nitrate (17, 18). The anaerobic response is mediated by the fnr gene product...

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“…1T,C-15G) with two mutations that render it growth rateindependent (8); and RLG1262 and RLG1259 contain a promoter from a ribosomal protein operon (spc) also shown previously to be growth rate-independent (7,31). Fig.…”

Section: Methodsmentioning

confidence: 99%

Guanosine 3'-diphosphate 5'-diphosphate is not required for growth rate-dependent control of rRNA synthesis in Escherichia coli.

Gaál

Gourse

1990

Proc. Natl. Acad. Sci. U.S.A.

109

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ABSTRACTrRNA synthesis in Escherichia coli is subject to at least two regulation systems, growth rate-dependent control and stringent control. The inverse correlation between rRNA synthesis rates and guanosine 3'-diphosphate 5'-diphosphate (ppGpp) levels under various physiological conditions has led to the supposition that ppGpp is the mediator of both control mechanisms by inhibiting transcription from rrn PI promoters. Recently, reL4 spoT-strains have been constructed in which both ppGpp synthesis pathways most likely have been removed (M. Cashel, personal communication). We have confirmed that such strains produce no detectable ppGpp and therefore offer a direct means for testing the involvement of ppGpp in the regulation of rRNA synthesis in vivo. Stringent control was determined by measurement of rRNA synthesis after amino acid starvation, while growth rate control was determined by measurement of rRNA synthesis under different nutritional conditions. As expected, the reL4-spoT-strain is relaxed for stringent control. However, growth rate-dependent regulation is unimpaired. These results indicate that growth rate regulation can occur in the absence of ppGpp and imply that ppGpp is not the mediator, or at least is not the sole mediator, of growth rate-dependent control. Therefore, growth rate-dependent control and stringent control may utilize different mechanisms for regulating stable RNA synthesis. rRNA synthesis constitutes a major fraction of the RNA synthesis in Escherichia coli. In cells growing under steadystate conditions, rRNA and tRNA synthesis rates are proportional to the square of the growth rate in order to meet the cell's requirements for protein synthesis, a phenomenon termed growth rate-dependent control (1-3). rRNA transcription is also subject to stringent control, a response to aminoacyl-tRNA limitation that results in severe inhibition of stable RNA (rRNA and tRNA) synthesis. rRNA synthesis is regulated primarily at the level of transcription initiation at the PI promoters of the seven rRNA operons (4-8). A negative feedback system responsive to the level of translationally competent ribosomes has been shown to control transcription from rrn PI and tRNA promoters (9-13) and has been proposed to be the mechanism for growth rate-dependent control (2, 7, 9).The role of the relA locus in the control of ribosome synthesis is a longstanding question in bacterial physiology (14). A rapid decline in stable RNA synthesis after amino acid starvation in relA' but not in relA-cells coincides with a large increase in the concentration of guanosine 3'-diphosphate 5'-diphosphate ("guanosine tetraphosphate," ppGpp; see refs. 15 and 16). The relA locus encodes ppGpp synthetase 1 (17). The relA system monitors the ratio of charged and uncharged tRNA at the ribosome, and upon amino acid starvation is responsible for the synthesis of -1000 pmol of ppGpp per ml per OD60 unit of cells (17)(18)(19)(20).In the absence of a functional relA locus, basal ppGpp levels (<100 pmolOD-ayml-') still vary inversely with...

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Growth-rate-dependent regulation of ribosome synthesis in E. coli: Expression of the lacZ and galK genes fused to ribosomal promoters

Cited by 97 publications

References 43 publications

Conserved features of coordinately regulatedE.colipromoters

Conserved features of coordinately regulatedE.colipromoters

Effect of cell growth rate on expression of the anaerobic respiratory pathway operons frdABCD, dmsABC, and narGHJI of Escherichia coli

Guanosine 3'-diphosphate 5'-diphosphate is not required for growth rate-dependent control of rRNA synthesis in Escherichia coli.

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