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Journal of Bacteriology, July 1999, p. 4245-4249, Vol. 181, No. 14
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Site-Specific Recombination of Bacteriophage P22
Does Not Require Integration Host Factor
Eun Hee
Cho,1,*
Chan-Eun
Nam,2
Renato
Alcaraz Jr.,3 and
Jeffrey F.
Gardner3
Department of Science Education1 and
Department of Genetic Engineering,2
Chosun University, Kwangju 501-759, Korea, and Department
of Microbiology, University of Illinois, Urbana, Illinois
618013
Received 2 August 1998/Accepted 31 March 1999
 |
ABSTRACT |
Site-specific recombination by phages 
and P22 is carried out by
multiprotein-DNA complexes. Integration host factor (IHF) facilitates
site-specific recombination by inducing DNA bends necessary to form
an active recombinogenic complex. Mutants lacking IHF are over
1,000-fold less proficient in supporting site-specific recombination than wild-type cells. Although the attP
region of P22 contains strong IHF binding sites, in vivo measurements
of integration and excision frequencies showed that infecting P22 phages can perform site-specific recombination to its maximum efficiency in the absence of IHF. In addition, a plasmid integration assay showed that integrative recombination occurs equally well in
wild-type and ihfA mutant cells. P22 integrative
recombination is also efficient in Escherichia coli in the
absence of functional IHF. These results suggest that nucleoprotein
structures proficient for recombination can form in the absence of IHF
or that another factor(s) can substitute for IHF in the formation of complexes.
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INTRODUCTION |
Bacteriophage P22 is a lambdoid
phage which infects Salmonella typhimurium. P22 can
integrate into and excise out of its host chromosome via site-specific
recombination. Both integration and excision reactions require the
phage-encoded int gene (29). Mutations of P22
affecting excision (xis mutants) are also known (32). Both the int and xis genes of
P22 have been sequenced (15).
Comparison of the deduced amino acid sequence of P22 Int with other
site-specific recombinases reveals that it is a member of the integrase family (1, 5, 22). The Int proteins of and P22
are composed of two domains. The catalytic domain binds to the core
region of the phage recombination site, attP, where the
actual recombination reactions occur. The smaller amino-terminal domain
binds to arm-type sequences which are located on either site of the
core within the attP (20, 30). The active
components of integrative and excisive recombination are
nucleosome-like structures, called intasomes, in which DNA is folded
around several molecules of Int and integration host factor (IHF)
(2, 8, 23, 26, 27). It has been demonstrated that one
monomer of integrase can simultaneously occupy both a core-type
binding site and an arm-type binding site (11, 16).
Formation of these bridges is facilitated by IHF, which binds to
specific sequences and imparts a substantial bend to the DNA (3,
25, 27, 31).
The attP regions of P22 and are also similar in that
both contain arm regions, known as the P and P' arms, which contain Int
arm-type binding sites and IHF binding sites (15, 30). However, the arrangement, spacing, and orientation of the Int and IHF
binding sites are distinct (30). The attP region
of contains two Int arm-type binding sites on the P arm and three on the P' arm. The P arm contains two IHF binding sites, and the P' arm
contains a single site. The attP region of P22 contains three Int arm-type binding sites on the P arm and two sites on the P'
arm. In addition, IHF binding sites, called H and H', are located on
each arm of the P22 attP. Leong et al. (14)
showed that the Escherichia coli IHF can recognize and bind
to these P22 IHF binding sites in vitro. It was also shown that the
maximum amount of P22 integrative recombination occurred in the
presence of E. coli IHF in vitro, whereas in its absence,
recombination was detectable but depressed (30). However,
the requirement for IHF or other possible accessory proteins during P22
site-specific recombination in vivo has not been tested. In this study,
we assessed the role of IHF in P22 integration and excision in vivo.
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MATERIALS AND METHODS |
Bacterial strains, media, chemicals, and enzymes.
The
bacterial strains used in this study are listed in Table
1. S. typhimurium JG1148 was
constructed by transduction of the
ihfA::tet insertion from NH560 into
MS1868 by selection for tetracycline resistance. The Tetr
cassette was inserted at the Lys-15 codon of the S. typhimurium ihfA gene (10a). E. coli JG1242 was
constructed by transduction of the Tn10-ihfA
82 allele
from KL1299 (7) and selection for tetracycline resistance.
The media and buffers used have been described previously
(
12). Luria-Bertani (LB) medium and Tris-EDTA (TE) buffer
were
made as described by Maniatis et al. (
18). All
antibiotics were
purchased from Sigma and used at the following
concentrations:
ampicillin, 100 µg/ml; kanamycin, 50 µg/ml; and
chloramphenicol,
20 µg/ml. Arabinose was obtained from Sigma and
added to a final
concentration of 1%. T4 DNA ligase and all
restriction endonucleases
were obtained from Gibco BRL.
Pfu
DNA polymerase was obtained
from
Stratagene.
Plasmid constructions.
Plasmids containing attP
sites of phages and P22 were derivatives of pJK4 (18a),
which contains oriR6K and a gene conferring resistance to
kanamycin (Kanr). The attP site was cloned
as a 267-bp PCR fragment ( positions 27569 to 27836) (4)
into the unique NlaIV site of pJK4 to create plasmid pRA102.
The P22 attP site was inserted into pJK4 by cloning a
1,034-bp PCR fragment (positions +725 to 
291) (14) into
the NlaIV site of pJK4. In addition, a copy of
lacPUV5
O+Z+Y+ from plac5
UV5 (24) was also inserted into the plasmid. The fragment carrying the lac genes was obtained by digestion of
phage DNA with KpnI and SphI ( positions 18568 and 23946) (4). It was purified and cloned into the unique
AvaII site of pJK4 to form plasmid pRA113. The
attP-containing fragments of both plasmids contain all of
the sequences necessary for or P22 integrative recombination in
vitro (28, 30).
The P22
int gene was cloned by PCR amplification of the gene
from bacteriophage P22 xis 2B (
21) by using
oligodeoxyribonucleotides
P22 Int-Top and P22 Int-Bot (Table
2). The amplified DNA contains
P22
sequences from position 62 to position 1216 (
15). The
oligodeoxyribonucleotides
introduced
KpnI and
PstI sites adjacent to the DNA encoding the
translation
initiation and termination codons of Int, respectively.
PCR DNA was
digested with
KpnI and
PstI and ligated into
pBAD33
DNA cleaved with the same enzymes to form the plasmid pIntP22.
The DNA upstream of the DNA encoding the translation initiation
codon
contains the natural ribosome binding site for P22
int.
The
lambda
int gene was cloned into pBAD33 as follows
(
33).
Oligodeoxyribonucleotides (IntXis1 and IntXis2 [Table
2]) complementary
to sequences 5' of the
xis gene and 3' of
the
int gene were used
for PCR amplification of the
int and
xis genes of
vir. The
resultant
fragment contained an
SphI site encoded by the
IntXis2 primer
downstream of the C terminus of
int. The
fragment was digested
with
XmnI (position 29015 in
xis) (
4) and
SphI, and then the
fragment was cloned into pBAD33 DNA digested with
SmaI and
SphI.
The construct contains part of
xis and the
natural translation
start signal upstream of
int. The
int genes of both pIntP22 and
pBMS10 were sequenced to
ensure that no PCR-induced errors occurred.
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TABLE 2.
Sequences of synthetic oligonucleotides for amplification
of P22 integrase attachment sites and cloning of int genes
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Integration and excision assays.
To measure integration,
MS1868 or JG1151 cells were grown in LB medium at 37°C to
mid-exponential phase, P22 phage were added to a multiplicity of
infection of 20 to 25, and the cell and phage mixtures were spread on
EBU plates (17) which were previously seeded with
109 PFU of P22 H5 (c2) (17).
Nonlysogens are killed by P22 H5, and only true P22 lysogens form light
green colonies.
Spontaneous excision was measured by growing lysogenic bacteria
overnight in LB medium followed by treatment with chloroform
and
centrifugation. Supernatants were diluted and spotted on a
lawn of
MS1868 to measure plaque formation. Excision of mid-exponential-phase
cells cultivated in LB medium was induced by adding mitomycin
to a
final concentration of 2 µg/ml. Cells were incubated at 37°C
with
aeration. After lysis, cell debris was centrifuged, and supernatants
were diluted and spotted against a lawn of MS1868 to measure plaque
formation.
Plasmid integration assays.
We developed a second
integration assay based on integration of a suicide plasmid containing
the P22 attP site. Integration of the
attP-containing plasmid pRA113 was used to measure the relative frequencies of integrative recombination in various host backgrounds (described above). The plasmid DNA was mixed with an equal
amount of pCKR101 (12) DNA, which carries an ampicillin resistance gene and a colE1 origin of replication. Cells
containing pIntP22 or pBAD33 were electroporated with 1 µl of the
plasmid mixture and grown for 1 h at 37°C in LB medium
supplemented with 1% arabinose. Dilutions were plated on LB agar
plates supplemented with 1% arabinose, chloramphenicol, and either
kanamycin or ampicillin. Because the strains lack Pi protein, which is
required for replication of pRA113, kanamycin-resistant colonies can
only arise by integration of the plasmid into the host chromosome. The
relative frequencies of integration are expressed as the ratio of
chloramphenicol- and kanamycin-resistant colonies (which contain
pIntP22 and have integrated pRA113) to chloramphenicol- and
ampicillin-resistant colonies (which contain pIntP22 and pCKR101).
Assays for integration performed with Int were done as described
for the P22 integration assay, except that cells contained pBMS10,
which expresses Int under PBAD control, and
pRA102 carrying attP was used as the integration
indicator plasmid.
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RESULTS AND DISCUSSION |
Isolation of a P22 derivative which does not require IHF for lytic
growth.
The ihfA and ihfB genes encode the
and 
subunits, respectively, of IHF. Phage P22 forms smaller
plaques on hosts carrying either ihfA or ihfB
mutations than on a wild-type host (12, 13). To measure the
extent of the IHF effect on lytic growth of P22, we compared single
burst sizes of P22 on a wild-type strain and an IHF-deficient strain.
The single burst size represents the number of progeny phage particles
which are produced from a single host cell infected by a single phage.
Infection of MS1868 (LT2 leuA414 hsdSB endE40) with P22
resulted in a single burst size of 196 PFU per cell, whereas infection
of an IHF-deficient host, JG1151 (MS1868 ihfA::tet
ihfB::cam) (12, 13), decreased the burst size
to 6 PFU per cell. This indicates that P22 does not grow lytically as
well in an IHF-deficient strain as in a wild-type strain, which is
consistent with an observation by Henthorn and Friedman
(10). To avoid complications due to IHF effects on the lytic
growth of P22, a derivative of P22 able to grow lytically in an
IHF-deficient strain was isolated as a mutant allele which formed
normal plaques on JG1151 (Table 1). The mutant, designated P22
goh5, which plaques with equal efficiency on both strains, was used in integration and excision assays in vivo.
P22 can integrate into the ataA site efficiently in the
absence of IHF.
To determine if IHF plays an important
architectural role during P22 integration in vivo, we measured the
lysogenization frequencies of wild-type P22 and P22 goh5 in
MS1868 and in JG1151. If IHF binding to the H and/or H' sites on the
P22 attP region is required, the lysogenization frequency of
P22 in the IHF-deficient host JG1151 would be lower than that of the
wild-type strain, MS1868. As shown in Table
3, the percent lysogeny of JG1151 upon
infection of both P22 wild-type phage and P22 goh5 was the
same as that of MS1868. This indicates that IHF in S. typhimurium is not an absolute requirement for the P22 integration
process in vivo.
We then tested whether the P22 prophages were inserted into the
specific bacterial attachment site,
ataA, in IHF-deficient
JG1151 (P22) lysogens by using PCR. Oligonucleotides B+ and B
were
designed to amplify the
ataA-containing region of the
S. typhimurium genome, and oligonucleotides P+ and P
were
designed
to amplify the
attP region of the phage P22 DNA
(Table
2). DNA
fragments containing
attL or
attR
can be amplified from a P22
lysogen when appropriate primer pairs were
used for PCRs: P+ and
B
for the
attL fragment and P
and
B+ for the
attR fragment.
DNA fragments containing the
attP region of P22 can be amplified
from P22 phage DNA or
from chromosomal DNA of multiple P22 lysogens.
Chromosomal DNA
templates which were purified from MS1868 nonlysogens,
MS1868(P22)
lysogens, or JG115 (P22) lysogens were amplified by
PCR. Both
MS1868(P22) and JG1151(P22) generated fragments containing
the
attL and
attR regions (Fig.
1, lanes 3 and 4 and 6 and 7).
No
fragments equivalent to the
ataA-containing fragments were
amplified when templates were purified from P22 lysogens (Fig.
1, lanes
9 and 10). The MS1868 nonlysogen only produced the
ataA-containing
fragment (Fig.
1, lanes 2, 5, and 8). This
result shows that the
P22 phage integrated into the same
ataA site in the IHF-deficient
strain as in the wild-type
S. typhimurium strain. None of the
three strains produced
the
attP-containing fragments (Fig.
1,
lanes 11 to 13),
which indicated those lysogens contained a single
prophage.
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FIG. 1.
PCR analysis to detect P22 prophage integrated into the
ataA site of S. typhimurium. PCR products were
analyzed by electrophoresis on a 1.5% agarose gel. The nucleotide
sequences of primers are shown in Table 2. Primer sets P+ and B, P
and B+, B+ and B, and P+ and P were used to amplify the 918-bp
attL-containing fragments, 362-bp attR-containing
fragments, 246-bp ataA-containing fragments, and 1,034-bp
attP-containing fragments, respectively (Table 2). DNA
templates were purified from MS1868 (lanes 2, 5, 8, and 11),
MS1868(P22) lysogen (lanes 3, 6, 9, and 12), JG1151(P22) lysogen (lanes
4, 7, 10, and 13), and P22 (lane 14). Lane 1 contains molecular size
markers, which are  X174 DNA digested with restriction enzyme
HaeIII. Samples were amplified with primers P+ and B
(lanes 2 to 4), P and B+ (lanes 5 to 7), B+ and B (lanes 8 to 10),
and P+ and P (lanes 11 to 14).
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We used a second assay based on integration of a plasmid containing P22
attP into the host
ataA site. The strains carry
pIntP22,
a pBAD33 (
9) derivative containing a copy of P22
int under
PBAD control, the pACYC184
origin of replication, and a gene encoding
resistance to
chloramphenicol. Integration of the plasmid pRA113
was used to measure
the relative frequencies of integrative recombination
in various host
backgrounds. It contains
oriR6K,
lacPuv5
O+ Z+ Y+, a copy of P22
attP, and a cassette conferring resistance to
kanamycin.
Because the strains lack Pi protein, which is required
for replication
of pRA113, kanamycin-resistant colonies can only
arise by integration
of the plasmid into the host chromosome.
The relative frequencies of
integration are expressed as the ratio
of chloramphenicol- and
kanamycin-resistant colonies (which contain
pIntP22 and have integrated
pRA113) to chloramphenicol- and ampicillin-resistant
colonies (which
contain pIntP22 and
pCKR101).
The results in Table
4 show that the
integration frequency of pRA113 is the same in both the wild type and a
strain carrying
an
ihfA::tet allele (JG1148
ihfA::tet). We also obtained the same
result with
strain NH560, which contains the original
ihfA::tet allele (data not shown). These results
are consistent with the
results from phage infections and further
support the conclusion
that integration requires Int but not IHF. We
did not detect integration
in a strain that contains the pBAD33 vector,
indicating that integration
is site specific.
We also tested P22
attP integration in isogenic
E. coli strains containing wild-type and mutant
ihfA
genes. Integration occurred
at the same frequency in both types of
cells (Table
4). In contrast,
integration of a plasmid containing
attP into the
attB site
of
E. coli and
the presumed
attB site in
S. typhimurium showed
a
marked dependence on IHF. Integration was decreased by approximately
5,000- and 500-fold in strains carrying mutant
ihfA alleles.
Prophage excision of P22 lysogen can proceed without IHF.
To
determine whether IHF plays a role in P22 excision in vivo, the number
of phage particles produced spontaneously after overnight cultivation
and upon mitomycin treatment of lysogens was measured. MS1868(P22)
produced more phage particles than the IHF-deficient lysogen,
JG1151(P22), under both conditions (Table 5). However, these values could represent
the effects of IHF on the two different processes
excisive
recombination of the prophage and the efficiency of lytic growth of the
excised P22 phage. The fact that MS1868(P22 goh5) and
JG1151(P22 goh5) produced the same level of viable phages
indicates that excision can occur with similar efficiencies in these
lysogens. Taken together, we conclude that the amount of excisive
recombination of P22 was not affected by the absence of IHF in vivo.
Is IHF in S. typhimurium involved in the site-specific
recombination of bacteriophage P22?
The site-specific
recombination systems of phages P22 and are similar in that they
are carried out by related integrases and that the attP
regions carry several Int arm-type binding sites and IHF binding sites
(14, 30). IHF binding sites on the attP region of
P22 were shown to be recognized by E. coli IHF
(14). In addition, E. coli IHF stimulates
recombination of P22 in vitro (30). We wanted to test
whether these two IHF binding sites are functional during the
site-specific recombination of P22 in vivo. The results showed that
neither the integration nor excision processes were affected by the
absence of IHF in vivo under the conditions used in this study. In
contrast, integration frequencies decreased dramatically in the
absence of IHF (Table 5) (19).
These results do not necessarily indicate that the two IHF binding
sites on the P22
attP site are dispensable. Although P22
site-specific recombination can proceed without IHF, there may
be
certain physiological conditions under which IHF facilitates
site-specific recombination of P22. In addition, the function
of IHF in
P22 site-specific recombination may be substituted for
by other
DNA-bending proteins in the host. It is possible that
such a protein
could be made by both
E. coli and
S. typhimurium,
because integration occurs in both hosts in the absence of IHF.
Goodman
et al. (
6) reported that the closely related protein
HU can
partially compensate for the function of IHF in
site-specific
recombination under some circumstances. We observed no difference
in
integration and excision frequencies of phage P22 in vivo in
a strain
deficient in HU production (data not shown). Further
studies and
comparison of the intasome structures of the two phages
will help us to
elucidate the structural and functional relationship
of the multiple
protein-DNA
complexes.
| |
ACKNOWLEDGMENTS |
We thank R. Kazmierczak, S. Maloy, M. Surber, and B. Swalla for
comments on the manuscript and J. Slauch, W. Metcalf, B. Swalla, and W. Reznikoff for strains.
This work was supported by KOSEF grant 951-0502-014-2 from Korea
Science and Engineering Foundation and NIH grant GM28717.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Science Education, Chosun University, Dong-gu, Seosuk-dong 375, Kwangju 501-759, Korea. Phone: 82-62-230-7370. Fax: 82-62-232-8122. E-mail: ehcho{at}chosun.ac.kr.
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Journal of Bacteriology, July 1999, p. 4245-4249, Vol. 181, No. 14
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
