Transcriptional Units for Ribosomal Proteins of Escherichia coli
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1 Eur. J. Biochem. 52, (1975) Transcriptional Units for Ribosomal Proteins of Escherichia coli Monica HIRSCH-KAUFFMANN, Manfred SCHWEIGER, Peter HERRLICH, Helmut PONTA, Hans-Jobst RAHMSDORF, Shou-Hsang PAI, and Heinz-Georg WITTMANN Max-Planck-lnstitut fur Molekulare Genetik, Berlin-Dahlem (Received September 7, 1974) Transcriptional units for ribosomal proteins in Escherichiu cofi were measured using the ultraviolet sensitivities of the rates of synthesis of individual ribosomal proteins. The ultraviolet sensitivities of gene transcriptions are proportional to the distances from the promoters. The longest transcriptional units for ribosomal proteins are 3.6 x 10' of DNA molecular weight corresponding to 1.8 x 10' of RNA or to of protein. The length would cover genes of ribosomal proteins (of an average M, of ). The synthesis of the ribosomal constituents seems to be highly coordinated. The coordinate control is suggested by the apparent constancy of ribosomes relative to growth rate [1,2] and the small pool of both the 55 individual ribosomal proteins [3] and the three ribosomal RNAs [4]. The mechanisms are unknown by which the synthesis of these many ribosomal components is regulated. An appealing possibility would be the arrangement of the ribosomal RNA genes in one transcriptional unit and of the ribosomal protein genes in another large transcriptional unit, a "ribosomal protein operon". The RNA genes indeed appear to be transcribed from the promoter in the order S - 5s RNA [4-71. The localization of many genes for ribosomal proteins in one region of the E. coli chromosome (between 64 and 66 min) [8] would be consistent with a ribosomal protein operon. It found further support by the polar effects of p-insertions on the expression of several ribosomal marker proteins [9]. However, experiments measuring the read-out time of mrna for ribosomal proteins after rifampicin addition, and the kinetics of synthesis of ribosomal proteins after rifampicin removal, indicated that not all genes for ribosomal proteins could be transcribed from one promoter [lo]. The experiments described here determine the size of the transcriptional units for ribosomal proteins by measuring the ultraviolet sensitivities of the rate of synthesis of the ribosomal proteins. It is shown that at least six transcriptional units for ribosomal proteins exist in E. coli, none of which carries more than ribosomal protein cistrons of average size. MATERIALS AND METHODS Radioactive and Other Chemicals ''C-labelled and 3H-labelled protein hydrolysate and ['4C]galactose were purchased from Radiochemicals, Amersham ; D-fucose was obtained from Sigma, St. Louis. Phage T7 wild type was grown and purified as described [I I]. Gro#tli of Bacteria E. coli Bs- [12] were grown at 30 "C in M9 medium supplemented with 0.4 % glucose and M MgSO,. Ultraviolet Irradiation At A600 = 0.35 the cells were irradiated in dim yellow light with various doses of ultraviolet light. 10-ml aliquots were placed in open glass petri dishes (r = 4.5 cm) under a 35-W ultraviolet lamp (Quarzlampenges. Hanau). The dose of irradiation was varied with the time of irradiation at a constant distance of 40 cm. The ultraviolet doses were roughly calibrated by comparing their effect on phage survival and on
2 470 E. coli Ribosomal Proteins : Transcriptional Units known phage marker genes [ll]. 25 s of ultraviolet reduced the surviving T7 phage of a suspension of the same A260 by lo3. The cultures were allowed to shake at 30 C for 10 min after the irradiation. Aliquots were then used for the following determinations : the rate of synthesis of galactokinase, the rate of synthesis of individual ribosomal proteins, and the rate of synthesis of various E. coli proteins. Rate of Synthesis of Various E. coli Proteins 0.2 ml aliquots of irradiated and non-irradiated cells were pulse-labelled with 14C-labelled amino acids (5 pci) for 5 min. A chase of 2 min with tryptone broth (1 % tryptone, 0.5% NaC1) followed. The cells were pelleted and treated with dodecylsulphate sample buffer [I 31. The total protein was separated by dodecylsulphate - polyacrylamide slab-gel electrophoresis [13]. The gels were dried and autoradiographed. The radioactivity in each protein band was determined by densitometry of the X-ray films. Galac tok inase Synthesis Galactokinase synthesis was determined by the rate of accumulation of enzyme activity upon induction with D-fucose. The enzyme was induced and assayed as described [14]. Rate of Synthesis of Individual Ribosomal Proteins 20-ml aliquots of irradiated and non-irradiated cells were made radioactive with 14C-labelled amino acids (1.24 pci/ml; 500 pci/pmol) for 5 min. The cells were harvested on ice and pelleted together with the same volume of 3H-labelled control cells. The control cells were not irradiated, but incubated with 3H-labelled amino acids (2.5 pci/ml; 1000 pci/pmol) for 15 min. Proteins were extracted with 67% acetic acid in the presence of 0.07 M magnesium acetate [15] from whole-cell homogenates (sonication) and resolved by the standard two-dimensional polyacrylamide gel electrophoresis [16]. In some cases carrier ribosomal protein was added before electrophoresis. The ribosomal protein spots were detected by staining with Coomassie blue and the radioactivity in each protein determined by cutting the spots out of the gel and separating 3H and 14C counts in a Packard autooxidizer. RESULTS AND DISCUSSION Principle of Promoter Mapping by Ultraviolet Irradiation Irradiation of whole cells with ultraviolet light interferes with replication and transcription. Both types of inhibition are caused by lesions in the DNA [17,18]. The ultraviolet lesions in the DNA cause termination of RNA chains prematurely under release of RNA polymerase. Ultraviolet lesions are distributed randomly; therefore, the probability to hit a stretch of DNA increases with its length : the target size. If transcription is observed, the transcriptional unit is the relevant target. The promoter-distal portion of a transcriptional unit is affected first and, with increasing doses of ultraviolet, the average length of transcribed RNA is reduced. From the portion beyond the ultraviolet lesion neither RNA nor protein is synthesized. The rate of synthesis of a protein thus is a measure of the surviving activity of the corresponding gene (provided that time is allowed to pass after the irradiation, so that preformed messenger can decay). Since, in most cases, it is difficult to define RNA species, the rate of synthesis of protein is determined. The ultraviolet sensitivity of transcription and subsequent translation depends on the distance of the end of the gene from its promoter. If a gene is located adjacent to the promoter, the ultraviolet sensitivity of its expression will be proportional to the molecular weight of the gene product. The ultraviolet sensitivity of a gene in a distal position of a transcriptional unit corresponds to the sum of the molecular weights of this gene product and of those proteins arising from promoter-proximal genes. The ultraviolet sensitivity is plotted as an inactivation curve and expressed as the inactivation tangent (as e.g. shown in Fig.3). The inactivation tangent is proportional to the target size, i.e. stretch of DNA transcribed. The inactivation tangent is plotted against the molecular weight (as in Fig. 2). This ultraviolet method has been worked out and tested in the bacteriophage T7 system [ll, 191. Ultraviolet Sensitivity of the Rate of Synthesis of Various E. coli Proteins In order to obtain a calibration curve for the ribosomal protein cistrons of E. coli, the ultraviolet sensitivity of the synthesis of various E. coli proteins was determined. Aliquots of cultures, which had been irradiated and which had been incubated subsequently for 10 min, were pulse-labelled with 14C-labelled amino acids and either used for the isolation and separation of ribosomal proteins, or directly for the separation of total protein by dodecylsulphate-polyacrylamide gel (Fig. 1). Even a superficial glance over autoradiograms of these gels shows that the proteins with high molecular weights disappear at lower doses ultraviolet irradiation than do those that had moved further in the gel. By densitometry of the autoradiograms the inactivation of synthesis by ultraviolet irradiation was
3 M. Hirsch-Kauffmann. M. Schweiger, P. Herrlich, H. Ponta, H.-J. Rahmsdorf, S.-H. Pai, and H.-G. Wittmann 471 / Fig. 1. Wltruriolet inuctirution of'thr rate qf'synthesis of E. coli proteins. E. coli Bs-, were irradiated with ultraviolet. The ultraviolet dose was varied by the time of irradiation under a source of constant ultraviolet light. After further incubation for 10 min, aliquots were taken for the following determinations: the rate of synthesis of galactokinase upon induction by D-fUCOSe (shown in Fig.2), the rate of synthesis of individual ribosomal proteins (Fig. 3 and Table I), and the rate of synthesis of various E. coli proteins. For the latter determination 0.2-ml aliquots were labelled with 5 pci "C-labelled amino acids. A chase with cold amino acids followed and the proteins were separated by dodecylsulphate- polyacrylamide slab-gel electrophoresis (10-20 "i, gradient). An autoradiogram is shown here. For standardization of the molecular weights, marker proteins were applied to the same slab gel. As an example, T7 proteins are shown (0-10-min pulse-label with '4C-labelled amino acids after infection of hcavily irradiated B,-, with T7'). All experiments of one set were performed with the same series of ultraviolet-irradiated cultures. 4 independent sets have been evaluated quantitated and the tangent plotted against the molecular weight, which was obtained by co-electrophoresis of marker proteins (Fig.2). The majority of proteins which were detected on dodecylsulphate gels plot on a straight line (Fig. 2). These proteins are apparently synthesized from genes that are located adjacent to promoters. Several proteins, however, show plot positions which are clearly above the line; for instance galactokinase synthesis, which was measured by its characteristic enzyme reaction, is inactivated at lower doses than would be expected from its molecular weight. The inactivation rate of galactokinase corre- I I I I IO-~ M, Fig. 2. Internul calihrcition standard for trunscriptionul-unit mapping with ultraviolet. As described in the text and as demonstrated in Fig. 3, inactivation curves for various proteins were obtained. Proteins were selected at random and only identified by their molecular weight. The slope of each curve, as a measure of the inactivation of the rate of synthesis by ultraviolet light, was expressed as the inactivation tangent, r. The tangent (a) of each protein was plotted against the molecular weight of the protein. The straight line served as a calibration curve as described in Results and Discussion. (0) Represents the value obtained for galactokinase synthesis. Galactokinase would have a molecular weight of if it were synthesized from a monocistronic transcriptional unit sponds to a DNA stretch of approximately x lo6 daltons or an RNA of 1.2 x lo6 daltons or a total protein of daltons. Galactokinase is coded by the third gene of the galactose operon [20]. Each of the three proteins of the gal operon has a molecular weight of [20] adding up to a total of The ultraviolet data thus say that all gal operon genes are transcribed from one promoter which has indeed been shown earlier by genetic methods [20]. With this plot we have obtained a calibration curve which was then used for the internal standardization of ultraviolet data with unknown transcriptional units, such as those for ribosomal proteins. Ultraviolet Sensitivity of the Rate of Synthesis of Individual Ribosomal Proteins The ribosomal proteins from E. coli have been isolated and their molecular weights have been
4 E. coli Ribosomal Proteins: Transcriptional Units lo I m I 1, 1 8 I c I Ultraviolet irradiation (5) Fig. 3. Ultraviolet sensitivit). oj the rute oj synthesis oj ribosomal proteins. After irradiation (see Fig. l), 20-ml aliquots of the cultures were pulse-labelled with 14C-labelled amino acids and mixed with control cells that had been labelled with 3H-labelled amino acids. The ribosomal proteins were separated and the rate of synthesis of each protein plotted as a percentage of control rate versus ultraviolet dose. The tangent a for each Ultraviolet irradiation ( s) protein was taken from these plots and evaluated in Table 1. (A) Example of proteins from the small ribosomal subunit; (B) examples of proteins from the large ribosomal subunit. The slope of inactivation of a gene, which is located at the end of a large transcriptional unit comprising all 55 ribosomal protein genes, is marked determined [21]. The average is to With this information, the ultraviolet method yields the size of the transcriptional unit or units. In order to measure rate of synthesis and not rate of assembly of ribosomal proteins, the ribosomal proteins were isolated from total-cell extracts (and not from isolated ribosomes) and separated by twodimensional gel electrophoresis. The locations of ribosomal proteins were detected by cochromatography of carrier protein and staining of the gels. The 14C counts (irradiated cells) in each spot were taken as a measure of the remaining synthesis rate as compared to the control rate (3H counts or 14C counts of nonirradiated sample). For each ribosomal protein ultraviolet-inactivation rates were plotted (Fig. 3). The theoretical curve for a unique operon containing all 55 ribosomal protein genes is marked. None of the inactivation rates of individual ribosomal proteins comes close to the curve calculated for the operon. The highest observed inactivation rate of an individual ribosomal protein was approximately 18-20% of that expected for the ribosomal operon. From the calibration curve (Fig. 2), the longest transcriptional unit has been calculated to be equivalent to 3.6 x lo6 daltons of DNA or 1.8 x lo6 daltons of RNA or about daltons of protein. At an average molecular weight of ribosomal proteins of to [21], the longest transcriptional unit would comprise about genes of average size. If all genes for ribosomal proteins were organized in such transcriptional units of maximal size, at least five transcriptional units would be needed for 55 ribosomal proteins. From the inactivation rates the relative positions of each gene with respect to its promoter were calculated (Table 1). As expected from the number of transcriptional units, at least six proteins exhibit ultraviolet sensitivities compatible with a location close to a promoter. Some of the ribosomal proteins with the lowest ultraviolet sensitivities of synthesis (such as L20) show at low doses of ultraviolet irradiation an increase of synthesis, and only at higher ultraviolet doses an inactivation (Fig. 3). These shoulders could be due to the inactivation of negative control mechanisms or simply reflect an artefact caused by the restriction of transcription to smaller stretches of DNA by the ultraviolet irradiation.
5 M. Hirsch-Kauffmann, M. Schweiger, P. Herrlich, H. Ponta, H.-J. Rahmsdorf, S.-H. Pai, and H.-G. Wittmann 473 Table 1. Distances of ribosomal protein genes from their promoters From the inactivation tangent data, such as those shown in Fig. 3, and from the calibration curve of Fig. 2, the distance of each gene from its promoter was obtained (in molecular weight of protein and of DNA that would correspond to the stretch between promoter and promoter-distal end of the gene). The data show good correlation in 4 independent experiments with the exception of those in brackets, which were more variable Protein s2 s3 s4 S6 s7 S8 s9 [SIO s11 [S13 S14 S15 S16 S17 S18 S19 s20 s21 L1 L2 L3 L4 L5 L6 L7 L8 L9 I L10 L11 L12 L13 L14 L15 L16 L17 L18 L19 L21 L22 [L23 L24 L25 L27 L29 L30 L32 Distance from promoter in DNA in protein (10-6 x M,) (10-3 x M,) The ultraviolet mapping of S18 is particularly interesting because S18 has been found by genetic methods to map at 84min [22], outside the region where other known ribosomal markers map. The ultraviolet sensitivity of S18 synthesis indicates that the gene for S18 is not close to a promoter. There would be space for four ribosomal protein genes or for other genes between the promoter and the S18 gene. The experiments reported here indicate the existence of several transcriptional units for ribosomal proteins. Our data are in agreement with those obtained by kinetic measurements [lo]. Our data would also explain the well-known flexibility of cells in the adjustment to nutrients and in the change of growth rate. At an average transcription rate of 50 nucleotides/s it would take 10min to express the whole ribosomal operon. The longest unit observed here would be expressed within 100 s. How the transcription of ribosomal protein cistrons is regulated is yet unknown. The ultraviolet data exclude, however, ribosomal RNA synthesis from being a controlling element. Because of the large size of the ribosomal RNA operon, ribosomal RNA synthesis is blocked at low doses of ultraviolet light, when little effect on the synthesis of ribosomal proteins was observed. REFERENCES 1. Maalqie, 0. (1969) Dev. Bid. Suppl. 3, Schleif, R. (1967) J. Mol. Biol. 27, Gausing, K. (1974) Mol. Gen. Genet. 129, Nikolaev, N., Silengo, L. & Schlessinger, D. (1973) Proc. Natl Acad. Sci. U.S.A. 70, Kossman, C. R., Stamato, T. D.&Pettijohn, D. E. (1971) Nut. New Biol. 234, Doolittle, W. F. & Pace, N. R. (1970) Nature (Lond.) 228, Bremer, H. & Berry, L. (1971) Nat. New Biol. 234, Osawa, S., Otaka, E., Takata, R., Dekio, S., Matsubara, M., Itoh, T. & Muto, A. (1972) in Functional Units in Protein Biosynthesis (Cox, R. A. & Hadjiolov, A. A., eds) pp , Academic Press, London. 9. Nomura, M. & Engback, F. (1972) Proc. Nut1 Acud. Sci. U.S.A. 69, Molin, S., von Meyenburg, K., Gullev, K. & Maalee, 0. (1974) Mol. Gen. Genet. 129, Herrlich, P., Rahmsdorf, H. J., Pai, S. H. & Schweiger, M. (1974) Proc. NatlAcad. Sci. U.S.A. 71, Hill, R. F. (1958) Biochim. Biophys. Acta, 30, Studier, F. W. (1973) J. Mol. Biol. 79, Williams. B. & Paigen, K. (1969) J. Bacterial. 97, Hardy, S. J. S., Kurland, C. G., Voynar, P. & Mom, P. (1969) Biochemistry, 8, Kaltschmidt, E. & Wittmann, H. G. (1970) Anal. Biochem. 36,
6 474 M. Hirsch-Kauffmann et al. : E. coli Ribosomal Proteins: Transcriptional Units 17. Michalke, H. & Bremer, H. (1969)J. Mol. Bid. 41, Wilson, D. B. & Hogness, D. S. (1974) J. Bid. Chrm. 18. Sauerbier, W., Millette, R. L. & Hackett, P. B. (1970) 244,2143. Biochim. Biophi~.s. Acta, 209, Dzionara, M., Kaltschmidt, E. & Wittmann, H. G. (1970) 19. Scherzinger. E.. Hcrrlich, P., Schweiger, H. & Schuster, H. Proc. Nut1 Acud. Sci. U.S.A. 67, (1972) Eui. J. Biochern. 25, Herzog, A,, C,abezon, T., Wilde, M. & Bollen, A. (1974) Mol. Gen. Genet. in press. M. Hirsch-Kauffmann, M. Schweiger, P. Herrlich, H. Ponta, H.-J. Rahmsdorf, S.-H. Pai, and H. G. Wittmann. Max-Planck-lnstitut fur Molekulare Genetik, D-1000 Berlin (West)-Dahlem 33, HarnackstraBe 23
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