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Journal of Bacteriology, December 2001, p. 6957-6960, Vol. 183, No. 23
Department of Molecular Biology, Umeå
University, S-901 87 Umeå, Sweden
Received 9 May 2001/Accepted 14 September 2001
In Saccharomyces cerevisiae, the rRNA Gm2270
methyltransferase, Pet56p, has an essential role in the maturation of
the mitochondrial large ribosomal subunit that is independent of its
methyltransferase activity. Here we show that the proposed
Escherichia coli ortholog, RlmB (formerly YjfH), indeed
is essential for the formation of Gm in position 2251 of 23S rRNA.
However, a The assembly of the 50S and
30S ribosomal subunits has been proposed to be a self-assembly process
as demonstrated by the ability to reconstitute in vitro fully active
ribosomes from the isolated components (36). However,
recent observations indicate that proteins that assist in the formation
of ribosomes, besides the ribosomal components, rRNA-processing
enzymes, and rRNA-modifying and ribosomal-protein-modifying
enzymes, have to be present in vivo. Indeed, there are at least seven
candidates in Escherichia coli: SrmB and DbpA, two DEAD box
RNA helicases (14, 15, 26, 33, 37, 46); Era, an essential
GTPase (30, 31-34, 41); RimM and RbfA, two proteins
associated with free 30S subunits but not with 50S subunits or 70S
ribosomes (5, 6, 10, 27); and DnaK and GroEL, two
molecular chaperones that at least at high temperature seem important
for ribosome maturation (1, 12, 42). Whether DnaK and
GroEL are directly or indirectly involved in the assembly of ribosomes
in E. coli is not known.
In Saccharomyces cerevisiae, the Pet56 protein catalyzes
2'-O-methylation at the universally conserved G at position
2270 (Gm2270) in the mitochondrial 21S rRNA (43),
corresponding to position 2251 of 23S rRNA of E. coli.
Further, pet56 null mutants lack functional mitochondrial
ribosomes, indicating that Pet56p is essential for the in vivo assembly
of the mitochondrial large ribosomal subunits (43).
Recently it was demonstrated that Pet56p variants with amino acid
substitutions in the SAM binding site, which abolished
methyltransferase activity, could support the in vivo assembly of
functional mitochondrial ribosomes, suggesting that Pet56p has a role
in ribosome assembly that is independent of its methyltransferase
activity (T. L. Mason, personal communication). In E. coli, the protein encoded by the yjfH gene is a
putative 2'-O-methyltransferase, based on its similarities
to other 2'-O-methyltransferases, especially Pet56p
(21). The yjfH gene in E. coli
encodes a hypothetical protein 243 amino acids in length and is
downstream from the rnr gene, encoding RNase R
(9). Just upstream from yjfH there are sequences that match those for promoters dependent on
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.23.6957-6960.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
The rlmB Gene Is Essential for
Formation of Gm2251 in 23S rRNA but Not for Ribosome Maturation in
Escherichia coli
ABSTRACT
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rlmB mutant did not show any ribosome
assembly defects and was not outgrown by a wild-type strain even after
120 cell mass doublings. Thus, RlmB has no important role in ribosome
assembly or function in E. coli.
TEXT
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70 for transcription initiation, and
downstream from yjfH there is a sequence characteristic of
rho-independent transcriptional terminators. To investigate whether
YjfH was the E. coli rRNA Gm2251 methyltransferase, a
chromosomal deletion of yjfH was constructed. The 835-bp
region upstream from yjfH was amplified by PCR using the
oligonucleotides rnr-F1 and yjfH-R1, trimmed
with HindIII and SalI, and cloned into the
temperature-sensitive plasmid vector pMAK705, yielding plasmid pMW458
(Table 1). The 917-bp region downstream
from yjfH was amplified by PCR using the oligonucleotides yjfH-F1 and yjfJ-R1, trimmed with
SalI and BamHI, and inserted into plasmid pMW458.
The resulting plasmid, pMW465, which contains an in-frame deletion that
covers all except the first two and last three codons of
yjfH replaced by a SalI site, was used to delete
the yjfH gene on the chromosome of strain MW100 following the procedure described by Hamilton et al. (23). One of
the resulting strains, MW244, was confirmed by PCR analyses to contain the yjfH deletion on the chromosome. A
yjfH+ strain, MW245, was isolated together
with MW244 and used as a control. Further, the
yjfH+ gene was amplified by PCR using the
oligonucleotides yjfH-F2 and yjfH-R2, trimmed
with EcoRI and HindIII, and cloned into
pBAD30, yielding plasmid pMW467. rRNA and tRNA from the
yjfH+ strain MW245, the yjfH
mutant MW244, and the mutant harboring the
yjfH+ plasmid pMW467 were prepared
(13), degraded with nuclease P1 and alkaline phosphatase
to nucleosides (17), and analyzed by high-pressure liquid
chromatography (HPLC) (16). The yjfH mutant MW244 did not show any deficiency in the modification of tRNA (data not
shown); however, it was found to lack Gm in 23S rRNA (Fig.
1B). This modification deficiency was
fully complemented by plasmid pMW467 (Fig. 1C). These findings and the
similarity of YjfH to Pet56p in S. cerevisiae, together with
the fact that in E. coli Gm is found in only one position in
rRNA, suggest that YjfH is indeed the E. coli rRNA Gm2251
methyltransferase. Therefore, we rename YjfH RlmB (for "rRNA
large-subunit methylation").
TABLE 1.
Bacterial strains, plasmids, and oligonucleotides
View larger version (16K):
[in a new window]
FIG. 1.
HPLC analysis of modified nucleosides in rRNA. Only the
part of the chromatograms that showed a difference between the strains
is shown. (A) Strain MW245 (rlmB+); (B)
strain MW244 ( rlmB); (C) strain MW244
(rlmB)/pMW467 (rlmB+). The
indicated nucleosides are 2'-O-methyl guanosine (Gm),
1-methyl guanosine (m1G), and 2-methyl guanosine
(m2G). The identity of Gm was confirmed by spectrum
analysis and by comparing the chromatograms with that for a
trmH::Kmr mutant lacking Gm in
tRNA (data not shown; see also reference 38).
RlmB is dispensable for fast growth.
To examine whether RlmB
is important for efficient growth, the growth rate at 37°C in
Luria-Bertani (LB) medium (2) was determined for the
rlmB mutant MW244 and the wild-type strain MW245. The
specific growth rate, k (= ln2/g, where
g is the mass doubling time in hours), of the
rlmB mutant was identical to that of the
rlmB+ strain (1.34; standard deviations of
0.021 and 0.031, respectively). Further, no difference between the two
strains was observed in their ability to grow at 21, 30, 37, and 44°C
on rich medium plates or at 30, 37, and 42.5°C on medium E plates
containing glucose. Also, stationary-phase cell culture density,
measured as optical density at 600 nm, and survival in stationary
phase, monitored by viable count determinations, after 24 and 48 h
of incubation at 37°C in LB medium did not differ between the two
strains (data not shown). To test the ability of the rlmB
mutant to grow in competition with the
rlmB+ strain over the whole range of the
growth cycle, the two strains were grown separately in LB medium at
37°C with shaking to stationary phase, at which the optical density
at 600 nm was 5.1 for both strains. Equal amounts of stationary-phase
cultures of mutant and wild-type cells were mixed, diluted
106-fold in LB medium, and incubated for 24 h. The dilution and incubation steps of the mixed culture were repeated
five times, and samples were taken at the start and after each cycle
and plated on rich medium. To determine the ratio of rlmB
cells to rlmB+ cells in the mixed culture,
48 colonies from each sampling time were subjected to PCR with
oligonucleotides rnr-F1 and yjfH-R2. Even after
six cycles, corresponding to more than 120 cell doublings, approximately 50% of the cells in the mixed culture were still rlmB mutants (data not shown). Thus, the lack of RlmB did
not confer any disadvantage to the mutant cells in their competition with rlmB+ cells.
RlmB is not important for ribosome maturation.
Since
pet56 mutants of S. cerevisiae that lack the rRNA
Gm2270 methyltransferase are deficient in the maturation of
mitochondrial large ribosomal subunits, we examined whether RlmB was
essential for assembly of ribosomes in E. coli. Polysome
extracts of strains MW244 (rlmB) and MW245
(rlmB+) were prepared (40) and
fractionated by sucrose gradient centrifugation (39). No
differences between the two strains were observed with respect to the
amounts of ribosomal subunits, 70S ribosomes, or polysomes (data not
shown). To detect any subtle deficiency in ribosome maturation of the
rlmB mutant, the kinetics of ribosome assembly were
studied by pulse-labeling techniques. Log-phase cultures of the two
strains grown in rich MOPS medium (35) lacking uracil were
labeled with [3H]uridine for 1 and 2 min.
Cellular extracts were prepared and analyzed by sucrose gradient
centrifugation under conditions that dissociated the 70S ribosomes into
50S and 30S subunits (29). The amounts of 50S subunit
assembly intermediates in the two strains were indistinguishable at
both 1 and 2 min of labeling (data not shown). Furthermore, when the
maturation of the 50S subunits was probed by primer extension analysis
of the 5' end of 23S rRNA (6), no increased accumulation
of precursors to 23S rRNA was observed in the rlmB mutant
(data not shown). These findings strongly suggest that RlmB is not
important for ribosome maturation in E. coli.
rlmB mutant studied here showed no
growth or ribosome assembly defects, Gm2251 cannot play any essential
role in ribosome assembly or function, which is also supported by
measurements of the peptidyltransferase activity of reconstituted
ribosomes containing in vitro-transcribed 23S rRNA lacking Gm2251
(18). However, we cannot exclude the possibility that
Gm2251 has some importance for ribosome function under conditions which
we have not tested. Our results also suggest that RlmB itself has no
important function in ribosome assembly. This contrasts with the
situation in S. cerevisiae, where the RlmB counterpart, Pet56p, has an essential function in the maturation of the
mitochondrial large ribosomal subunit that is independent of its
methyltransferase activity (43; Mason, personal
communication). In comparison to RlmB, Pet56p has an N-terminal
extension of 143 amino acids. Conceivably, the maturation function of
Pet56p might reside in this part of the protein, explaining why the
rlmB mutant was not deficient in ribosome maturation.
This maturation function might be completely absent in E. coli or might be performed by another protein or by 23S rRNA.
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ACKNOWLEDGMENTS |
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We thank Kerstin Jacobsson for analyzing RNA by HPLC. We are grateful to Thomas L. Mason for communicating data on Pet56p prior to publication. We thank Olof P. Persson, Glenn R. Björk, and Tord G. Hagervall for stimulating discussions and comments on the manuscript.
This work was supported by the Swedish Natural Science Research Council (B-BU 9911), the Carl Trygger Foundation, and the Magnus Bergvall Foundation.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Molecular Biology, Umeå University, S-901 87 Umeå, Sweden. Phone: 46-90-7856754. Fax: 46-90-772630. E-mail: Mikael.Wikstrom{at}micro.umu.se.
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Journal of Bacteriology, December 2001, p. 6957-6960, Vol. 183, No. 23
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.23.6957-6960.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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