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Journal of Bacteriology, November 1999, p. 6822-6827, Vol. 181, No. 21
Department of Biotechnology,
Received 17 June 1999/Accepted 13 August 1999
A DNA fragment carrying the genes coding for EcoO109I
endonuclease and EcoO109I methylase, which recognize the
nucleotide sequence 5'-(A/G)GGNCC(C/T)-3', was cloned from the
chromosomal DNA of Escherichia coli H709c. The
EcoO109I restriction-modification (R-M) system was found to
be inserted between the int and psu genes from
satellite bacteriophage P4, which were lysogenized in the chromosome at
the P4 phage attachment site of the corresponding leuX gene
observed in E. coli K-12 chromosomal DNA. The
sid gene of the prophage was inactivated by insertion of
one copy of IS21. These findings may shed light on the
horizontal transfer and stable maintenance of the R-M system.
Escherichia coli
H709c has been widely used as an antigenic tester strain of the
E. coli O109 group, and the serotype formula of this strain
was established as O109:K( To date, about 150 type II restriction-modification (R-M) genes have
been cloned and their nucleotide sequences have been analyzed
(27). The genes coding for endonuclease and
methyltransferase are closely linked on either chromosomal DNA or
plasmid DNA. Of the 167 type II R-M enzymes isolated from E. coli, 11 genes have been cloned and their nucleotide sequences
have been analyzed. The EcoRI (22),
EcoRV (3), EcoRII (16), and
Eco29kI (40) systems are encoded by plasmid DNA,
whereas the EcoHK31I (17) system is encoded by
chromosomal DNA. The characterization of type II R-M systems has shown
that some systems contain other components in addition to the requisite
endonuclease and methyltransferase. One of these is the C element,
which is known to activate R expression in the BamHI and
PvuII R-M systems (12, 33). Genes encoding proteins involved in DNA mobility, such as transposases, integrases, and invertases, are sometimes found in the vicinity of R-M systems located on chromosomal DNA (1, 5, 13, 17, 31, 35). These
proteins might facilitate the transfer of R-M genes among different
bacterial strains.
In this study, we report the cloning and characterization of the
EcoO109I R-M system and the location of the system on the chromosome. The nucleotide sequence adjacent to the R-M system has led
to interesting speculation about the evolutionary history of
EcoO109I.
Purification of R.EcoO109I and
M.EcoO109I.
R.EcoO109I and
M.EcoO109I were partially purified from the cell extracts by
combined chromatography on DEAE-Sephacel, phosphocellulose, hydroxylapatite, and heparin-Sepharose. When the peak fractions were
electrophoresed on a sodium dodecyl sulfate (SDS)-polyacrylamide gel,
R.EcoO109I and M.EcoO109I produced major bands of
32.5 and 45 kDa, respectively. The corresponding bands were blotted
onto a polyvinylidene difluoride membrane (20) and then
subjected to N-terminal amino acid sequence analysis. The first 20 amino acids of R.EcoO109I and M.EcoO109I obtained
on Edman degradation were
Met-Asn-Lys-Gln-Glu-Val-Ile-Leu-Lys-Val-Gln-Glu-Xxx-Ala-Ala- Trp-Trp-Ile-Leu-Glu
and
Ser-Ser-Lys-Lys-Phe-Ile-Ser-Leu- Phe-Ser-Gly-Ala-Met-Gly-Leu-Xxx-Leu-Gly-Leu-Gln (Xxx, not
identified), respectively.
Isolation of EcoO109I R-M genes.
To isolate the
two genes, oligonucleotide N1 (Table 1)
was synthesized from the N-terminal amino acid sequence of
R.EcoO109I and used as a probe for Southern hybridization
with E. coli H709c chromosomal DNA digested with various
restriction endonucleases. The 4.8-kb BglII fragment was
cloned into the BamHI site of the pUC118 vector to obtain
pUC-B1. The purified plasmid DNA from the clone was digested with
R.EcoO109I, and the plating efficiency of Nucleotide and deduced amino acid sequences.
The DNA sequence
of the 3.1-kb EcoT22I fragment that covers the entire
EcoO109I R-M gene is shown in Fig.
2. The two open reading frames (ORFs)
were aligned tail to tail, and a 38-bp spacer region was found between
them. A putative palindromic sequence, which is found in the
StsI R-M system (15), was seen within the spacer
region; this could be the transcriptional termination site for both
genes. In the ORF assigned to the endonuclease gene, an ATG codon
appeared at nucleotide position 762 and a termination codon at
nucleotide position 1578. In addition, an appropriate ribosome-binding
sequence, GGA, was present 11 bp upstream of the ATG codon. The ORF
consisted of 816 bp and encoded a 272-amino-acid-residue polypeptide.
The predicted mass, 31,435 Da, was close enough to the value estimated
on SDS-polyacrylamide gel electrophoresis. R.EcoO109I exhibits identity with R.SinI
(13) and R.Eco47I (31), which
recognize G
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Evidence of Horizontal Transfer of the
EcoO109I Restriction-Modification Gene to Escherichia
coli Chromosomal DNA
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):H19 by Ørskov et al. (23). A type II restriction endonuclease,
R.EcoO109I, which recognizes and cleaves the nucleotide
sequence of 5'-(A/G)G
GNCC(C/T)-3', has been isolated from E. coli H709c (21). It has been reported that
R.EcoO109I cleavage is inhibited by the modification of the outer cytosine in the recognition sequence (29). However,
neither the position nor the products of methylation by the cognate
methyltransferase, M.EcoO109I, have been determined yet.
virulent phage
for the cells carrying pUC-B1 was the same as that for control cells
carrying no plasmid. These results suggested that a partial, i.e., not
the complete, EcoO109I R-M gene was located on the 4.8-kb
BglII fragment. In order to find longer DNA fragments
carrying genes encoding complete EcoO109I R-M enzymes within
the E. coli H709c chromosomal DNA, the 9-kb BamHI
fragment was cloned into the BamHI site of the EMBL3
vector to obtain EMBL3-25. DNA was purified from the phage, and the
5.8-kb EcoRV-BamHI fragment was analyzed in
detail (Fig. 1). The 3.1-kb
EcoT22I fragment was inserted into the PstI site
of pKF3 and the resulting recombinant plasmid, pKF3-1, was transferred
to E. coli TH2. R.EcoO109I activity in the cell
extract was assayed at 37°C by adding 2 µl of enzyme solution to 15 µl of reaction mixture (10 mM Tris-HCl [pH 7.5], 10 mM
MgCl2, 1 mM dithiothreitol, and 0.5 µg of T4
cytosine-containing DNA [dC DNA]). M.EcoO109I activity was
assayed as the susceptibility of pKF3-1 to R.EcoO109I. The
colonies carrying the plasmid expressed both endonuclease and
methyltransferase activities. These results indicated that the 3.1-kb
region is essential for encoding both the restriction endonuclease and
the methyltransferase.
TABLE 1.
Bacterial strains, plasmids, phages,
and oligonucleotides
View larger version (13K):
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FIG. 1.
Restriction map of the 9-kb BamHI fragment.
The positions and orientation of the R.EcoO109I
(ecoO109IR) and M.EcoO109I (ecoO109IM)
genes, as well as those of ORF1, ORF2, and ORF3, are indicated by
arrows.
G(A/T)CC, and R.Sau96I (32) and
R.Eco47II (31), which recognize G GNCC.
View larger version (85K):
[in a new window]
FIG. 2.
Nucleotide sequence of the 3,142-bp EcoT22I
fragment. The amino acid sequences assigned to ecoO109IR and
ORF1 are given below the nucleotide sequence, and the sequence assigned
to ecoO109IM is given above the nucleotide sequence. The
nucleotide sequence is numbered from the leftmost end, and the amino
acid sequences of ecoO109IR and ecoO109IM are
numbered from the initiation codon of each gene. The potential
ribosome-binding sequences are dotted. A pair of arrows indicates
palindromic sequences characteristic of the termination signal.
Sequences flanking the R-M system. Two additional ORFs (ORF1 and ORF2) and one ORF (ORF3) were discovered upstream of the R.EcoO109I and the M.EcoO109I genes, respectively. ORF1 (303 bp) was discovered upstream of the R.EcoO109I gene and partially overlaps the gene. A molecular mass of 11,455 Da is in good agreement with the predicted sizes of other C proteins, which associate with several type II R-M systems and regulate the expression of R-M genes (1, 37). ORF1 appears to be distantly related to known C proteins but shows homology to the DNA-binding domains of various regulatory proteins (18, 36, 38). The role of ORF1 is under investigation.
One ORF (ORF2; 1,284 bp), which showed significant homology to the integrase from the P4 phage (9), was identified upstream of ORF1. Furthermore, BLAST searches of the GenBank database revealed that a DNA sequence similar to that of the P4 phage attachment site followed by the E. coli K-12 MG1655 leuX gene (2) was found upstream of the int gene. The 190-amino-acid polypeptide (ORF3) encoded upstream of the M.EcoO109I gene also exhibited similarity with the psu gene product from the P4 phage. The DNA upstream of M.EcoO109I also contains sequences that exhibit identity with the cos sequence and
genes from the P4 phage. From
these results, we assumed that the DNA of the hybrid P4 phage, in which the cII, 
, and gop genes were replaced by R-M
genes (including ORF1), was inserted into E. coli H709c
chromosomal DNA through site-directed recombination catalyzed by P4 integrase.
In order to confirm that the complete P4 genes, except for the
cII, , and gop genes, were inserted into the
E. coli H709c chromosome, we synthesized several
oligonucleotides based on the DNA sequence of P4 phage DNA and used
them for PCR (Table 1). PCR was carried out with ExTaq DNA
polymerase and an LA-PCR kit (Takara Shuzo Co. Ltd., Kyoto, Japan) as
recommended by the manufacturer. The lengths of the fragments amplified
from E. coli H709c DNA with the -N, -C, sid-N bottom,
and Att oligonucleotides were the same as expected from the nucleotide
sequence. The restriction profiles of these fragments were the same as
expected. However, the fragments amplified with the -C and Att
oligonucleotides were 2 kb longer than expected. These results
suggested the possibility of rearrangement or insertion of a new
sequence into the sid gene. The nucleotide sequence of the
3-kb DNA fragment amplified with the sid-C and sid N-top
oligonucleotides was analyzed, and it was shown that one copy of
IS21 (25) was inserted between nucleotides 312 and 313 in the top strand and between nucleotides 308 and 309 in the
bottom strand of the sid gene, which generated a frameshift mutation of the sid protein. The results are summarized in
Fig. 3.
|
Absence of type I R-M genes and a methylation-specific restriction system in E. coli H709c. E. coli has been shown to contain type I R-M systems, such as EcoK, EcoB, and EcoIC, as well as restriction systems requiring modification, such as Mcr and Mrr. In order to determine whether or not E. coli H709c possesses one of those genes for type I R-M systems and systems requiring modification, in addition to the type II EcoO109I R-M system, we amplified these genes by PCR. Primers based on the nucleotide sequence of E. coli K-12 MG1655 were designed to amplify these genes (Table 1). DNA fragments of the expected sizes were amplified from E. coli W3110 DNA but not from E. coli H709c or E. coli XL-1 Blue MRF' DNA. These results suggested that E. coli H709c did not contain the EcoK, mcrABC, and mrr genes, which are present in E. coli K-12 derivatives.
There have been several reports of the close association between enzymes involved in DNA mobility and R-M systems. A partial P4 phage int gene occurs next to the R.SinI (13), M.EcoHK31I, and M.EaeI genes (17); a partial integrase gene of retronphage
R73 also
occurs next to the R.EaeI gene (11, 17); and a
gene for the Int family of recombinases occurs 3' to the
M.AccI gene (5). A gene for a DNA invertase-like
enzyme is found near the M.PaeR7I (35) gene, and
the transposon resolvase gene is located upstream of the
R.BglII gene (1). A putative transposase-encoding gene is found in the intergenic area between the R.Eco47I
and M.Eco47II genes (31). These enzymes are
supposed to facilitate the transfer of the R-M systems among bacterial species.
We found that complete P4 phage genes, other than the cII,
, and gop genes, were lined up in a sequential order
adjacent to the EcoO109I R-M system. Furthermore, a DNA
sequence similar to that of the P4 phage attachment site, followed by
E. coli K-12 MG1655 chromosomal DNA, was found upstream of
the int gene. Comparison of the G+C contents of the
sequenced regions of the EcoO109I R-M system, including ORF1
and the surrounding system, revealed an interesting feature: although
the overall G+C content of P4 phage DNA was 49%, the genes in the
EcoO109I R-M system had an average G+C content of 36%. This
indicates that the P4 phage was lysogenized in the E. coli
H709c chromosome at the P4 attachment site observed in E. coli K-12, in which genes nonessential for lytic growth, i.e., the
cII, , and gop genes, were replaced by
EcoO109I R-M genes, including ORF1.
P4 can complete its life cycle only if it infects a cell that already
has a helper phage, such as P2, within it or if a helper phage is
supplied later. This means that P4 acts as a satellite phage or a
parasite. We have found that one copy of IS21 was inserted in the sid gene, which generates a frameshift mutation of
the sid protein. The sid gene product is supposed
to be responsible for determining the precise size and symmetry of the
structure into which the helper P2 gene products will assemble.
Inactivation of the P4 sid gene does not necessarily prevent
the formation of plaques, and the mutant produces P4 PFU with large
P2-sized capsids which contain two or three copies of the mutant P4
genome (30).
P4 can inject its own DNA into E. coli and other
gram-negative bacteria, such as Salmonella and
Klebsiella (19). When P4 infects a sensitive
E. coli host harboring the genome of helper phage P2, it may
enter either the lysogenic or lytic pathway, being dependent on all the
morphopoietic and lytic functions encoded by the helper to accomplish
the latter mode of replication. In the absence of the helper phage,
infection of E. coli by P4 may lead to either an
immune-integrated condition, analogous to the lysogenic state, or the
establishment of the multicopy plasmid mode of maintenance. This
property, as well as P4's genetic organization, suggests that P4 may
be considered an episomal element that evolved the ability to exploit a
helper bacteriophage for horizontal propagation through a novel
specialized transduction mechanism (19). These data are
consistent with the following hypothesis for the transfer of the
EcoO109I R-M system to the chromosome DNA. First, a hybrid P4, in which the cII, , and gop genes were
replaced by EcoO109I R-M genes, was produced through
bacterial recombination. Second, the bacteria carrying the hybrid P4
were infected by a helper phage, such as P2, and thus the P4 phage
particles were released. Third, E. coli H709c was infected
by the hybrid P4 phage, and the P4 DNA was integrated into the
chromosome. Finally, the sid gene was inactivated by the
insertion of IS21, and the prophage carrying the
EcoO109I R-M system was maintained stably on the chromosome.
It is conceivable that migration of the R.EcoO109I gene
alone is not unfavorable for the P4 phage because of the lack of a
target site of R.EcoO109I in its DNA (9) but is
lethal for the host cell. It is quite interesting that the
int genes found in four of seven R-M systems were similar to
those of P4 and related R73 phages. Extensive analysis of the
nucleotide sequences adjacent to other R-M systems will provide clues
to the evolution and migration of the R-M systems in bacteria.
Nucleotide sequence accession number. The GenBank accession number for the DNA sequence of the gene encoding the EcoO109I R-M system is AF157599.
| |
ACKNOWLEDGMENTS |
|---|
E. coli H709c was obtained from M. Miyahara (Institute of Public Health, Tokyo, Japan).
This work was supported in part by a Grant-in-Aid for Scientific Research on Priority Areas (no. 296) from the Ministry of Education, Science, Sports and Culture, Japan.
| |
FOOTNOTES |
|---|
* Corresponding author. Mailing address: Department of Biotechnology, Tottori University, 4-101 Koyama, Tottori 680-8552, Japan. Phone: 81-857-31-5277. Fax: 81-857-31-0881. E-mail: kita{at}bio.tottori-u.ac.jp.
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Journal of Bacteriology, November 1999, p. 6822-6827, Vol. 181, No. 21
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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