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J Bacteriol. 2000 May; 182(10): 2893–2899.
PMCID: PMC102000

Growth Phase-Coupled Changes of the Ribosome Profile in Natural Isolates and Laboratory Strains of Escherichia coli


The growth phase-dependent change in sucrose density gradient centrifugation patterns of ribosomes was analyzed for both laboratory strains of Escherichia coli and natural isolates from the ECOR collection. All of the natural isolates examined formed 100S ribosome dimers in the stationary phase, and ribosome modulation factor (RMF) was associated with the ribosome dimers in the ECOR strains as in the laboratory strain W3110. The ribosome profile (70S monomers versus 100S dimers) follows a defined pattern over time during lengthy culture in both the laboratory strains and natural isolates. There are four discrete stages: (i) formation of 100S dimers in the early stationary phase; (ii) transient decrease in the dimer level; (iii) return of dimers to the maximum level; and (iv) dissociation of 100S dimers into 70S ribosomes, which are quickly degraded into subassemblies. The total time for this cycle of ribosome profile change, however, varied from strain to strain, resulting in apparent differences in the ribosome profiles when observed at a fixed time point. A correlation was noted in all strains between the decay of 100S ribosomes and the subsequent loss of cell viability. Two types of E. coli mutants defective in ribosome dimerization were identified, both of which were unable to survive for a prolonged period in stationary phase. The W3110 mutant, with a disrupted rmf gene, has a defect in ribosome dimerization because of lack of RMF, while strain Q13 is unable to form ribosome dimers due to a ribosomal defect in binding RMF.

During the growth transition of bacteria from exponential to stationary phase, the expression of growth-related genes is mostly turned off and instead a set of genes required for stationary-phase survival is switched on (19, 23, 24). For this drastic change in gene expression pattern, structural and functional modulations take place on both transcriptional and translational apparatuses (23, 24). Previously, we identified a 100S form of ribosome dimers in stationary-phase Escherichia coli cells and the association of a small basic protein of 55 amino acid residues, ribosome modulation factor (RMF), with those ribosome dimers (47). RMF is one of the stationary-phase-specific gene products (47, 51), and the rmf mutant strain loses cell viability in stationary-phase culture more rapidly than the wild-type strain (51). The addition of RMF to 70S ribosomes promotes their conversion in vitro into 100S dimers and inhibits translation in vitro (46), supporting the idea that the 100S dimers are a storage form for ribosomes in stationary phase (46, 51).

In order to explore this hypothesis, we have examined the relationship between the formation of ribosome dimers and the fate of E. coli cells. Up to the present time, data concerning stationary-phase adaptability and its variation among E. coli strains have been obtained using a small number of E. coli laboratory strains. It is noted, however, that the laboratory strains often carry mutations in the genes which are expressed only in the stationary phase, probably because these strains have never been exposed to lengthy culture. Surprisingly, some laboratory strains contain mutations that inactivate the RNA polymerase ςS subunit (25), which is required for recognition of some stationary-phase-specific gene promoters (19, 23, 24). In this study, we have analyzed some representative strains from the ECOR collection, which comprises a set of 72 E. coli reference strains isolated from a variety of animal hosts and geographical locations (34), as well as some laboratory strains with or without mutations affecting the ability to undergo ribosome dimerization.

Previously, the growth characteristics of some of the ECOR strains as well as some fresh natural isolates were compared with the kinetic properties of their ribosomes in vitro (30, 31, 35). The variability in the kinetic parameters characteristic of ribosome functions indicates that there is no unique wild-type ribosome phenotype nor is there a unique growth phenotype for the bacteria. As an extension of this line of study, we have carried out a systematic analysis of the time-dependent change in ribosome patterns for some of the ECOR strains. The results described here indicate that the overall pattern of ribosome profile change is similar among strains but that the total length of time for this cycle of ribosome change differs from strain to strain. Since the decrease in 100S ribosome dimers is always accompanied by the initiation of cell death, we propose that the cycle of ribosome profile change is closely related to the life cycle of E. coli. This relationship was tested for two different types of E. coli mutant defective in ribosome dimerization, one devoid of RMF and the other carrying mutant ribosomes defective in binding RMF.


Bacterial strains and culture.

The bacterial strains used were 19 representatives (Ecor2, -11, -16, -20, -28, -32, -36, -42, -43, -46, -48, -49, -52, -57, -60, -62, -63, -64, and -68) from the ECOR collection and some laboratory strains, including W3110 lineage A (25), Q13 (43), and HMY15, lacking the rmf gene (51). Overnight cultures in Luria-Bertani (LB) medium were inoculated into 1.7 liters of fresh LB medium, and the cells were grown at 37°C with shaking at 100 cycles per min with a TAITEC MM-10 water bath shaker (Koshigaya, Japan). This shaking speed gave maximum stationary-phase survival for most E. coli strains. In time course analyses of ribosome profiles during lengthy culture, medium E (44) supplemented with 2% polypeptone was also used.

Preparation of ribosomes.

Cells were ground with an approximately equal volume of quartz sand and extracted with Noll's buffer I (10 mM Tris-HCl [pH 7.6], 10 mM magnesium acetate, 100 mM ammonium acetate, and 6 mM 2-mercaptoethanol) (33). Preparation of both crude and high-salt-washed ribosomes from the cell extracts was carried out essentially according to the method of Noll et al. (33) with slight modification as described by Wada (45).

Sucrose gradient centrifugation of ribosomes.

Ribosomes were fractionated by sucrose density gradient centrifugation as described previously (22, 45). Samples were layered on top of a 5 to 20% (wt/vol) sucrose gradient in ribosome buffer (20 mM Tris-HCl [pH 7.6], 15 mM magnesium acetate, and 100 mM ammonium acetate) and centrifuged in a Hitachi RPS50-2 rotor at 40,000 rpm for 80 min at 4°C. After centrifugation, the absorbance of sucrose gradients at 260 nm was measured with a Shimadzu (Kyoto, Japan) UV200 spectrophotometer using a flow cell.

Two-dimensional electrophoresis of ribosomal proteins.

Ribosomal proteins were prepared from total cell extracts or ribosomes by the acetic acid method (17). After dialysis against 2% acetic acid, the proteins were lyophilized and stored at −80°C until use. The radical-free and highly reducing (RFHR) method of two-dimensional gel electrophoresis (45) was used for analysis of ribosomal proteins after slight modification as described by Wada et al. (47).


Ribosome pattern differences among E. coli isolates from the ECOR collection.

We chose 19 strains from the 72 different isolates of the ECOR collection and used them for an analysis of growth-dependent variation in ribosome profiles. The ECOR strains have been classified into several groups on the basis of pattern differences in multilocus enzyme electrophoresis (34, 40). The 19 strains were selected from these groups, i.e., A, B1, B2, C, and D (for the selected strains, see Materials and Methods). The growth rate was determined for each of the 19 strains cultured by shaking at 37°C in medium E (44) supplemented with polypeptone. The growth rate (GR) varied 2.4-fold, ranging from 0.39 (strain Ecor52) to 0.92 (Ecor29) doublings per h. The maximum saturation density (SD) (A660) in medium E ranged from 0.5 (Ecor11) to 3.8 (Ecor16). Previously, Mikkola and Kurland (32) analyzed the growth rate of nearly the same set of E. coli strains in glucose-limited chemostats and found that the maximum growth rates were 0.48 to 1.43 doublings per h, giving about a threefold difference between the lowest and the highest rates of cell growth. The range and order of growth rate differences among the test E. coli strains measured in medium E were essentially the same as those determined in the glucose-limited chemostats. The analysis of evolution in vitro of natural isolates of E. coli in glucose-limited chemostats indicated that, after 280 generations, the maximum growth rates of all the cultures approximated that of standard laboratory wild-type strains, which was close to 1.33 doublings per h (32). We confirmed the increase in the growth rate of ECOR strains after repeated cultures in LB medium with shaking. Thus, it appears that slow growth is characteristic of natural E. coli isolates.

After overnight culture of a laboratory E. coli strain, W3110, we found that ribosomes are converted into 100S dimers by binding RMF, which is synthesized during the growth transition of E. coli from exponential to stationary phase (47, 51). After transfer of the overnight culture into a fresh medium, the 100S ribosome dimers were converted into 70S monomers within a few minutes (47). The ribosome profile was then analyzed for the overnight culture of the 19 ECOR strains grown in LB medium. Ribosomes from all 19 strains analyzed formed two peaks, one corresponding to 70S monomers and the other component sedimenting faster than the 70S monomers (see below). The content of ribosome dimers relative to monomers varied among the 19 natural isolates (data not shown). One group of strains formed high levels of the ribosome dimers, while the dimer content in another group of ECOR strains was less than the monomer content. The apparent difference in the ribosome profile at a fixed time of cell culture might be due to the difference in cell growth phase, because the cell growth rate is significantly different among strains (see above).

Time course of ribosome pattern change in natural isolates.

Previously, we analyzed the change in ribosome profiles during overnight culture of some laboratory E. coli strains (46). Here we examined the ribosome profiles during lengthy culture of the ECOR strains. For comparison, we chose some representative strains with different levels of ribosome dimers at the culture time of 24 h. In the time course experiments, medium E (43) supplemented with 2% polypeptone was used instead of LB medium because the bacterial life span is generally longer in medium E. The test strains were cultured at 37°C for a prolonged time (up to 1 week) with constant shaking. Growth was monitored by measuring the turbidity, while the viable counts were measured on LB plates. Ribosomes were prepared at various growth phases of the culture and analyzed by sucrose density gradient centrifugation. Figure Figure11 shows the ribosome profiles for four strains, Ecor68 (GR, 0.75 doublings per h; SD [A600], 3.4) Ecor48 (GR, 0.50; SD, 2.6), Ecor11 (GR, 0.78; SD, 0.5), and Ecor16 (GR, 0.65; SD, 3.8). The time-dependent change in sedimentation behavior of ribosomes was found to be essentially the same in all of the strains, consisting of four stages: (i) formation of 100S dimers in the early stationary phase, (ii) transient decrease in the dimer level, (iii) return of dimers to the maximum level, and (iv) dissociation of 100S dimers into 70S ribosomes, which are quickly disassembled into subassemblies (Fig. (Fig.1;1; also see Fig. Fig.33 for the ribosome profile of W3110). The duration of this cycle of ribosome profile change, however, varied from strain to strain.

FIG. 1
Growth phase-coupled change in ribosome profile. Four representative ECOR strains, Ecor68, Ecor48, Ecor11, and Ecor16, were grown in medium E supplemented with 2% polypeptone. At the indicated times (5 h to 6 days [d]) after transfer ...
FIG. 3
Growth phase-coupled changes in the ribosome profile and the cell viability of strain W3110. (A) Turbidity (squares) was measured at 660 nm, while cell viability (circles) was measured on LB agar plates. (B) Based on the growth-coupled changes in the ...

The level of 100S ribosome dimers in Ecor68 is high in the early stationary phase (5 h) and then decreases at a culture time of 10 h, followed by the second peak of ribosome dimers at days 1 to 3. The time-dependent changes in the ribosome patterns of Ecor48 and Ecor16 are essentially the same as that of Ecor68, but the rate of disappearance of ribosome dimers at the final stage is faster than with Ecor68. In the case of Ecor11, the levels of ribosome dimers at both the first (5 h) and second (days 1 to 3) peaks are lower than those of the other three test strains. The time course for the loss of 100S dimers was faster for strains Ecor48, Ecor11, and Ecor16. At day 4, the 100S dimer level was less than 10% of the total ribosomes. The lack of ribosome dimers was immediately followed by the complete disappearance of intact ribosomes at day 5. Viable cells were markedly reduced at this time point.

To examine whether the formation of ribosome dimers in natural E. coli isolates also depends on the association of RMF, as was observed for the laboratory strains (47, 51), we performed two-dimensional gel electrophoresis of total ribosomal proteins from the ECOR strains by the RFHR method, which was developed for better resolution of basic proteins (45, 47). RMF was detected only in the 100S dimer fractions of all four strains examined (data not shown; Fig. Fig.22 shows the protein composition of strain W3110), but except for the RMF content, little difference was found in the stained gel patterns of ribosomal proteins, at least until the middle of stationary phase. Thus, we concluded that the difference in ribosome patterns was closely correlated with the association of RMF. This is consistent with the in vitro reconstitution experiment of 100S ribosomes from RMF and 70S ribosomes (46).

FIG. 2
Growth phase-coupled change in the ribosome profile of strain W3110 and the two-dimensional gel pattern of its ribosomal proteins. E. coli W3110 was grown in medium E supplemented with 2% polypeptone. The sucrose density gradient centrifugation ...

Time course of ribosome profile change in laboratory strains.

Since a close correlation exists between the loss of ribosome dimers and the initiation of bacterial cell death, one possible triggering factor for cell death might be the dissociation of ribosome dimers. In order to test this relationship in detail and to identify possible alterations in the protein composition of ribosomes other than the association of RMF, we analyzed the growth phase-dependent changes of the ribosome profile and the two-dimensional gel pattern of ribosomal proteins for some E. coli laboratory strains with defined genetic backgrounds. First, we analyzed strain W3110 lineage A, which we used for analysis of the growth-dependent changes in the RNA polymerase pattern (25) and nucleoid protein composition (42). Under the same culture conditions described above, the W3110 cells retained high levels of the 100S ribosome dimers until day 4 (Fig. (Fig.2).2). At day 5, the amount of ribosome dimers decreased again to 20 to 25% of the maximum level. At day 6, not only 100S dimers but also most 70S monomers disappeared. The viable count at day 6 was about 10% of the maximum level. At day 7, virtually no viable cells were detected (less than 1%). Overall, the patterns of growth phase-dependent changes in the ribosome profile were essentially the same in the natural isolates and the laboratory strain, but the time required for one cycle of ribosome change varied from strain to strain.

On the basis of the ribosome profile change, the stationary phase of E. coli culture can be divided into four stages, as summarized in Fig. Fig.3.3. Stage I corresponds to the early stationary phase, characterized by the initial accumulation of 100S ribosome dimers, which is followed by a transient decrease in 100S ribosomes in stage II. The decrease of 100S ribosomes is accompanied by the synthesis of some stationary-phase proteins for adaptation to a dormant stage for prolonged survival (see Discussion). The level of 100S dimers again increases in stage III. The viable counts decrease in the early stationary phase, but afterward the total number of viable cells remains constant until stage III. In stage IV, the level of 100S ribosomes starts to decrease concomitantly with the decrease of viable counts. The total time period for this life cycle of bacteria depends on the medium composition and is different in different bacterial strains. During such a lengthy culture under the conditions employed, the medium pH showed a typical change, characterized by the initial decrease in early stationary phase to about 5.5 and then the gradual increase to about 8.5 after day 5.

The change in the composition of ribosomal proteins in strain W3110 was followed during the time course of prolonged culture. The level of RMF, determined as the value relative to those of L27, L29, and L30, which all migrated near RMF on the two-dimensional gel, decreased concomitantly with the disappearance of 100S dimers. When the total amount of RMF was divided by the total amount of 70S ribosomes present in the 100S dimers, the molar content of RMF per 70S ribosome unit was found to range from 0.8 to 0.9 in stages I and II to 1.2 to 1.4 in stage III, supporting the prediction that each 100S dimer is associated with two molecules of RMF (or each 70S unit in the dimers contains one molecule of RMF). Since the total amount of RMF per dimer-associated 70S ribosome unit increased above 1 in the middle of stationary phase, it appears that a fraction of RMF exists in a free unassembled state. At present, it remains unresolved whether the unassembled RMF exists in vivo or represents an artifact due to dissociation of ribosomes during isolation of the ribosome dimers.

In the course of the analysis of ribosomal proteins, we noticed several other changes in ribosomes: (i) the level of ribosomal protein S22, the spot D protein according to the RFHR gel (45), always increases three- to fivefold in the stationary phase (Fig. (Fig.4C);4C); (ii) multiple forms (S3′ and S3") of the ribosomal protein S3 can be detected only in the exponential phase (Fig. (Fig.4C);4C); (iii) the ribosomal protein L16 is cleaved, in some cases, into fragments in stationary-phase ribosomes, and only the N-terminal proximal fragments (L′ and L") are associated with ribosomes (Fig. (Fig.2);2); (iv) the ribosomal protein L35, the spot A protein in the RFHR gel (45), is sometimes dissociated concomitantly with the cleavage of L16 (Fig. (Fig.2);2); (v) the ribosomal proteins L7/L12 are the last components associated with ribosome subassemblies during degradation (Fig. (Fig.2).2). Since these changes were observed in late stationary phase and for both monomeric and dimeric forms of ribosomes, the changes in ribosomal proteins might not be associated with ribosome dimerization.

FIG. 4
Mutants defective in ribosome dimerization. (A) E. coli Q13 was grown in medium E supplemented with 2% polypeptone. At various culture times as indicated, cell lysates were prepared as described in Materials and Methods and immediately subjected ...

Mutants defective in the formation of ribosome dimers.

We next analyzed mutants defective in ribosome dimerization, in which RMF is involved (46, 47). This involvement was strongly supported by the finding that ribosome dimers could not be detected for RMF null mutants (51). We followed the cell growth and ribosome profile during lengthy culture of mutant HMY15, with rmf deleted (51). As shown in Fig. Fig.4D,4D, no ribosome dimers were found throughout the culture from exponential to late stationary phase. At day 4, viability had already decreased to 15% as measured by colony formation, and at day 5, virtually no colony formers were detected.

After a search for laboratory strains defective in ribosome dimerization, we found that strain Q13 did not form 100S dimers (47). The strain Q13 is widely used for RNA analysis because it lacks ribonuclease A and polynucleotide phosphorylase (43). After lengthy culture of strain Q13, we confirmed the lack of ribosome dimers and reduced viability in stationary phase. To identify the defective mechanism of ribosome dimerization in the Q13 strain, we analyzed the ribosomal proteins by two-dimensional gel electrophoresis. RMF was not detected at either exponential or stationary phase (Fig. (Fig.4C).4C). To confirm that the defect in ribosome dimerization in strain Q13 is attributable to the absence of RMF, an attempt was made at in vitro reconstitution of ribosome dimers by the exogenous addition of RMF. As shown in Fig. Fig.4B,4B, the ribosome dimer was not formed. Under the same reconstitution conditions, however, the 70S ribosomes from E. coli W3110 were converted into 100S dimers by the addition of RMF (data not shown), as we observed previously (46). This observation raised the possibility that the Q13 ribosomes are defective in binding RMF. Taken together, these data led to the conclusion that ribosome dimers are not formed in strain Q13 because the ribosomes are defective in binding RMF (and because of the lack of RMF production). Since rmf mRNA could be detected in strain Q13 (51), one possibility is that unassembled RMF is rapidly degraded.

The two types of E. coli mutant defective in ribosome dimerization both showed shorter lifetimes in stationary phase than the wild-type strains.


Most of what we know about genotypic and phenotypic variation in E. coli has been derived from studies of laboratory strains. For instance, the response of bacteria to environmental stresses has been analyzed for the most part using a small number of laboratory strains (for reviews, see references 23 and 24). The molecular mechanisms observed in such model systems may be different from those expressed by natural isolates. For example, some E. coli W3110 stocks lack ςS and/or ςF subunits of RNA polymerase (25). Even though these ς factors are required for transcription of some stress response genes, the relevant stress conditions may normally be absent from laboratory culture conditions, and thus the defective bacterial stocks can be maintained in captivity.

The ECOR collection, a set of 72 reference strains of E. coli isolated from a variety of hosts and geographical locations, was established by Ochman and Selander (34) and has been widely used in studies of variation in natural isolates. Such studies have focused on diverse characteristics of the bacterial genome (1, 49, 11, 12, 14, 15, 17, 18, 21, 36, 37, 39, 41, 48), on the distributions of branched DNA-RNA molecules (20), and on variations in the complexities of protein families (3, 7, 13, 16, 29, 38, 49, 50). Previously, Mikkola and Kurland (31) analyzed ribosomes from translation mutants as well as some natural isolates of E. coli. The results indicated that bacteria harboring kinetically impaired ribosomes increase the number of ribosome particles accumulated under poor growth conditions in order to compensate for their defective function. Some of the kinetic characteristics of ribosomes are different among original natural isolates. After growth in glucose-limited chemostats, however, the ribosomes of all of the cultures become kinetically indistinguishable from those of laboratory wild-type bacteria. Thus, bacteria grown under normal laboratory conditions have been selected for maximum growth rates, and this in turn demands maximum translation efficiency (32). In contrast, maximum growth rates do not seem to be strongly selected for in the ECOR collection of natural isolates (30).

In rapidly growing E. coli strains, ribosomes are involved in dynamic cycles of translation. Upon entry into the stationary phase, the step time of the functional ribosome cycle is delayed, and as a result, the level of translation frameshift by ribosomal slippage is markedly increased (2, 10). Excess unused ribosomes are converted into translationally inactive 100S dimers (46, 47). Although a number of changes take place in parallel both in the composition and pH of media and in intracellular compositions in stationary-phase E. coli culture, the ribosome dimerization might be primarily due to the association of RMF, because (i) ribosome dimers can be reconstituted even from chemically synthesized RMF and exponential phase 70S ribosome dimers (46) and (ii) ribosome dimers are not formed in vivo in the absence of RMF (51). The structural and functional modulations of ribosomes appear to be required for prolonged survival in the stationary phase. The RMF null mutants showed reduced viability in stationary phase (51). Reduced viability was also observed for the E. coli Q13 strain (Fig. (Fig.4A),4A), which does not form ribosome dimers, presumably due to a ribosomal defect in binding RMF (Fig. (Fig.4A4A and B).

As in the case of translation machinery, RNA polymerase appears to be stored in inactive form in the stationary phase. The core enzyme forms complexes with polyphosphate (28), and the ς70 subunit for transcription of growth-related genes forms a complex with the anti-sigma factor RSD (regulator of sigma D) (26, 27; also reviewed in references 23 and 24). Thus, in the stationary phase, both translation and transcription apparatuses are converted into inactive stored forms, which can be reused upon reentry into the growth cycle. Since the disassembly of 100S ribosomes is immediately accompanied by degradation of 70S ribosomes, ultimately leading to cell death, it appears that the initiation of 100S ribosome disassembly triggers switching to cell death. Alternatively, an as-yet-unidentified common factor may simultaneously trigger both ribosome disassembly and cell death.


This work was supported by grants-in-aid from the Ministry of Education, Science, Culture and Sports of Japan and CREST (Core Research for Evolutionary Science and Technology) of Japan Science and Technology Corporation (JST).


1. Anton A I, Martinez-Murcia A J, Rodriguez-Valera F. Sequence diversity in the 16S-23S intergenic spacer region (ISR) of the rRNA operons in representatives of the Escherichia coli ECOR collection. J Mol Evol. 1998;47:62–72. [PubMed]
2. Barak Z, Gallant J, Lindsley D, Kwieciszewki B, Heidel D. Enhanced ribosome frameshifting in stationary phase cells. J Mol Biol. 1996;263:140–148. [PubMed]
3. Barcus V A, Titheradge A J B, Murray N E. The diversity of alleles at the hsd locus in natural populations of Escherichia coli. Genetics. 1995;140:1187–1197. [PMC free article] [PubMed]
4. Bingen E, Picard B, Brahimi N, Mathy S, Desjardins P, Elion J, Denamur E. Phylogenetic analysis of Escherichia coli strains causing neonatal meningitis suggests horizontal gene transfer from a predominant pool of highly virulent B2 group strains. J Infect Dis. 1998;177:642–650. [PubMed]
5. Blackwood R A, Rode C K, Pierson C L, Bloch C A. Pulse-field gel electrophoresis genomic fingerprinting of hospital Escherichia coli bacteraemia isolates. J Med Microbiol. 1997;46:506–510. [PubMed]
6. Boyd E F, Hartl D L. Nonrandom location of IS1 elements in the genome of natural isolates of Escherichia coli. Mol Biol Evol. 1997;147:725–732. [PubMed]
7. Boyd E F, Hartl D L. Chromosomal regions specific to pathogenic isolates of Escherichia coli have a phylogenetically clustered distribution. J Bacteriol. 1998;180:1159–1165. [PMC free article] [PubMed]
8. Boyd E F, Hill C W, Rich S M, Hartl D L. Mosaic structure of plasmids from natural populations of Escherichia coli. Genetics. 1996;143:1091–1100. [PMC free article] [PubMed]
9. Desjardins P, Picard B, Kaltenbock B, Elkion J, Denamur E. Sex in Escherichia coli does not disrupt the clonal structure of the population: evidence from random amplified polymorphic DNA restriction-fragment-length polymorphism. J Mol Evol. 1995;41:440–448. [PubMed]
10. Fu C, Parker J. A ribosomal frameshifting error during translation of the argI mRNA of Escherichia coli. Mol Gen Genet. 1994;243:434–441. [PubMed]
11. Garcia-Martinez J, Martinez-Murcia A J, Anton A I, Rodriguez-Valera F. Comparison of the small 16S and 23S interegenic spacer region (ISR) of the rRNA operons of some Escherichia coli strains of the ECOR collection and E. coli K-12. J Bacteriol. 1996;178:6374–6377. [PMC free article] [PubMed]
12. Garcia-Martinez J, Martinez-Murcia A J, Rodriguez-Valera F, Zorraquino A. Molecular evidence supporting the existence of two major groups in uropathogenic Escherichia coli. FEMS Immunol Med Microbiol. 1996;14:231–244. [PubMed]
13. Goullet P, Picard B. Comparative electrophoretic polymorphism of esterases and other enzymes in Escherichia coli. J Gen Microbiol. 1989;135:135–143. [PubMed]
14. Green L, Miller R D, Dukhuizen D E, Hartl D L. Distribution of DNA insertion element IS5 in natural isolates of Escherichia coli. Proc Natl Acad Sci USA. 1984;81:4500–4504. [PMC free article] [PubMed]
15. Hall B G, Parker L L, Betts P W, DuBose R F, Sawyer S A, Hartl D L. IS103, a new insertion element in Escherichia coli: characterization and distribution in natural populations. Genetics. 1989;121:423–431. [PMC free article] [PubMed]
16. Hall B G, Sharp P M. Molecular population genetics of Escherichia coli: DNA sequence diversity at the celC, crr, and gutB loci of natural isolates. Mol Biol Evol. 1992;9:654–665. [PubMed]
17. Hardy S J, Kurland C G, Voynow P, Mora G. The ribosomal proteins of Escherichia coli. I. Purification of the 30S ribosomal proteins. Biochemistry. 1969;8:2897–2905. [PubMed]
18. Hartl D L, Sawyer S A. Why do unrelated insertion sequences occur together in the genome of Escherichia coli? Genetics. 1988;118:537–541. [PMC free article] [PubMed]
19. Hengge-Aronis R. Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli. Cell. 1993;72:165–168. [PubMed]
20. Herzer P J, Inouye S, Inouye M, Whittam T S. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol. 1990;172:6175–6181. [PMC free article] [PubMed]
21. Hill C W, Feulner G, Brody M S, Zhao S, Sadosky A B, Sandt C H. Correlation of rhs elements with Escherichia coli population structure. Genetics. 1995;141:15–24. [PMC free article] [PubMed]
22. Horie K, Wada A, Fukutome H. Conformational studies of Escherichia coli ribosomes with the use of acridine orange as a probe. J Biochem. 1981;90:449–461. [PubMed]
23. Ishihama A. Modulation of the nucleoid, the transcription apparatus, and the translation machinery in bacteria for stationary phase survival. Genes Cells. 1999;3:135–143. [PubMed]
24. Ishihama A. Adaptation of gene expression in stationary phase bacteria. Curr Opin Genet Dev. 1997;7:582–588. [PubMed]
25. Jishage M, Ishihama A. Variation in RNA polymerase sigma subunit composition within different stocks of Escherichia coli strain W3110. J Bacteriol. 1997;179:959–963. [PMC free article] [PubMed]
26. Jishage M, Ishihama A. A stationary phase protein in Escherichia coli with binding activity to the major ς subunit of RNA polymerase. Proc Natl Acad Sci USA. 1998;95:4953–4958. [PMC free article] [PubMed]
27. Jishage M, Ishihama A. Transcriptional organization and in vivo role of the Escherichia coli rsd gene, encoding the regulator of RNA polymerase sigma D. J Bacteriol. 1999;181:3768–3776. [PMC free article] [PubMed]
28. Kusano S, Ishihama A. Functional interaction of Escherichia coli RNA polymerase with inorganic polyphosphate. Genes Cells. 1997;2:433–441. [PubMed]
29. Marklund B-I, Tennent J M, Garcia E, Harmers A, Baga M, Lindberg F, Gaastra W, Normark S. Horizonal gene transfer of the Escherichia coli pap and prs operons as a mechanism for the development of tissue-specific adhesive properties. Mol Microbiol. 1992;6:2225–2242. [PubMed]
30. Mikkola R, Kurland C G. Is there a unique ribosome phenotype for naturally occurring Escherichia coli? Biochimie. 1991;73:1061–1066. [PubMed]
31. Mikkola R, Kurland C G. Evidence for demand-regulation of ribosome accumulation in E. coli. Biochimie. 1991;73:1551–1556. [PubMed]
32. Mikkola R, Kurland C G. Selection of laboratory wild-type phenotype from natural isolates of Escherichia coli in chemostats. Mol Biol Evol. 1992;9:394–402. [PubMed]
33. Noll M, Hapke B, Noll H. Structural dynamics of bacterial ribosomes. II. Preparation and characterization of ribosomes and subunits active in the translation of natural messenger RNA. J Mol Biol. 1973;90:519–529. [PubMed]
34. Ochman H, Selander R K. Standard reference strains of Escherichia coli from natural populations. J Bacteriol. 1984;157:690–693. [PMC free article] [PubMed]
35. Rang C U, Mikkola R, Molin S, Conway P L. Ribosomal efficiency and growth rates of freshly isolated Escherichia coli strains originating from the gastrointestinal tract. FEBS Lett. 1997;418:27–29. [PubMed]
36. Riley M A, Gordon D M. A survey of Col plasmids in natural isolates of Escherichia coli and an investigation into the stability of Col-plasmid lineages. J Gen Microbiol. 1992;138:1345–1352. [PubMed]
37. Saluta M V, Hirshfield I N. The occurrence of duplicate lysyl-tRNA synthetase gene homologs in Escherichia coli and other procaryotes. J Bacteriol. 1995;177:1872–1878. [PMC free article] [PubMed]
38. Sandt C H, Wang Y-D, Wilson R A, Hill C W. Escherichia coli strains with nonimmune immunoglobulin-binding activity. Infect Immun. 1997;65:4572–4579. [PMC free article] [PubMed]
39. Sawyer S A, Dykhuizen D E, DuBose R F, Green L, Mutangadura-Mhlanga T, Wolczyk D F, Hartl D L. Distribution and abundance of insertion sequences among natural isolates of Escherichia coli. Genetics. 1987;115:51–63. [PMC free article] [PubMed]
40. Selander P K, Korhonen T K, Vaisanen-Rhen V, Williams P H, Pattison P E, Caugant D A. Genetic relationships and clonal structure of strains of Escherichia coli causing neonatal septicemia and meningitis. Infect Immun. 1986;52:213–222. [PMC free article] [PubMed]
41. Smith D K, Kassam T, Singh B, Elliot J F. Escherichia coli has two homologous glutamate decarboxylase genes that map to distinct loci. J Bacteriol. 1992;174:5820–5826. [PMC free article] [PubMed]
42. Talukder A A, Iwata A, Nishimura A, Ueda A, Ishihama A. Growth phase-dependent variation in the protein composition of Escherichia coli nucleoid. J Bacteriol. 1999;181:6361–6370. [PMC free article] [PubMed]
43. Thang M N, Thang D C, Grunberg-Manago M. An altered polynucleotide phosphorylase in E. coli Q13. Biochem Biophys Res Commun. 1967;28:374–379. [PubMed]
44. Vogel H J, Bonner D M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1986;218:97–106. [PubMed]
45. Wada A. Analysis of Escherichia coli ribosomal proteins by an improved two dimensional gel electrophoresis. I. Detection of four new proteins. J Biochem. 1986;100:1583–1594. [PubMed]
46. Wada A, Igarashi K, Yoshimura S, Aimoto S, Ishihama A. Ribosome modulation factor: stationary growth phase-specific inhibitor of ribosome functions from Escherichia coli. Biochem Biophys Res Commun. 1995;214:410–417. [PubMed]
47. Wada A, Yamazaki Y, Fujita N, Ishihama A. Structure and probable genetic location of a “ribosome modulation factor” associated with 100S ribosomes in stationary-phase Escherichia coli cells. Proc Natl Acad Sci USA. 1990;87:2657–2661. [PMC free article] [PubMed]
48. Wang F-S, Whittam T S, Selander R K. Evolutionary genetics of the isocitrate dehydrogenase gene (icd) in Escherichia coli and Salmonella enterica. J Bacteriol. 1997;179:6551–6559. [PMC free article] [PubMed]
49. Wang Y-D, Zhao S, Hill C W. Rhs elements comprise three subfamilies which diverged prior to acquisition by Escherichia coli. J Bacteriol. 1998;180:4102–4110. [PMC free article] [PubMed]
50. Wanner B L, Boline J A. Mapping and molecular cloning of the phn (psiD) locus for phosphonate utilization in Escherichia coli. J Bacteriol. 1990;172:1186–1196. [PMC free article] [PubMed]
51. Yamagishi M, Matsushima H, Wada A, Sakagami M, Fujita N, Ishihama A. Regulation of the Escherichia coli rmf gene encoding the ribosome modulation factor: growth phase- and growth rate-dependent control. EMBO J. 1993;12:625–630. [PMC free article] [PubMed]

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