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Previous Article | Next Article 
Journal of Bacteriology, January 2001, p. 405-409, Vol. 183, No. 1
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.1.405-409.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
areCBA Is an Operon in
Acinetobacter sp. Strain ADP1 and Is Controlled by AreR, a
54-Dependent Regulator
Rheinallt M.
Jones and
Peter A.
Williams*
School of Biological Sciences, University of
Wales Bangor, Bangor, Gwynedd LL57 2UW, Wales, United Kingdom
Received 12 July 2000/Accepted 12 October 2000
 |
ABSTRACT |
The areCBA genes in Acinetobacter sp.
strain ADP1, determining growth on benzyl alkanoates, are shown to be
transcribed as a single operon and regulated by areR, which
encodes a regulatory protein of the NtrC/XylR family. Assays of the Are
enzymes and of two insertions of lacZ as a reporter gene
have shown that the operon is induced by benzyl acetate, benzyl
alcohol, and benzaldehyde, as well as 2- and 4-hydroxybenzyl acetates
and benzyl propionate and butyrate. Two adjacent sites of
transcriptional initiation were 97 and 96 bp upstream of the start
codon for areC, near a 
54-dependent 
12,
24 promoter. Inactivation of areR and rpoN
(for RNA polymerase 54) drastically reduced growth rates
on the Are substrates and induction of the operon.
| |
TEXT |
The areC, -B,
and -A genes in Acinetobacter sp. strain ADP1 are
located (9, 10) in a 30-kbp supraoperonic cluster of catabolic genes which includes the ben and cat
genes encoding the enzymes of the catechol branch of the
-ketoadipate pathway (5, 6, 7, 17, 19). The
are genes (Fig. 1) encode an
esterase and two dehydrogenases, responsible for the sequential catabolism of benzyl alkanoates to benzoate, salicylate, or
4-hydroxybenzoate, respectively (Fig. 2),
which feed into the -ketoadipate pathway (9, 10).
Sequence analysis of areC, -B, and -A
and the promoter region suggests that they may be cotranscribed and
expressed as an operon (9), upstream of which is a gene
designated areR (homologous to genes encoding
transcriptional activators of the NtrC/XylR family [16,
18] and a possible regulator of the putative operon).
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FIG. 1.
Physical map of the DNA adjacent to the ben
genes in ADP1. Physical map of the areCBA genes and their
locations relative to one end of the supraoperonic ben-cat
cluster. The various inserts of the plasmids produced from cloning
genomic DNA into vectors are specified in Table 1. Plasmids named in
boldface contain inserts that were cloned directly from genomic DNA.
All other plasmids were produced by PCR from genomic DNA or by
subcloning from plasmids containing genomic DNA. Sites at the termini
of the inserts marked with an asterisk were incorporated via PCR
primers. The Km cassette or lacZ-Km cassette insertions are
not to scale. The abbreviations for the restriction sites are Bc,
BclI; Bg, BglII; E, EcoRI; H,
HindIII; N, NsiI; P, PstI; S,
SacI; X, XbaI.
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Table 1 lists the plasmids and bacterial
strains used in this study. The latter were cultivated as previously
described (9). Aromatic substrates were obtained as
previously described (9). Standard methods for DNA
manipulations and plasmid preparation (20) or previously
described methods (9) were used. Growth of cells was
monitored, and preparation of cell extracts and assays of Are enzymes
was conducted, as described previously (9). -Galactosidase in lysed cells was determined using the method described by Miller (15). The promoterless
lacZ-Km cassette was removed from pKOK6.1 (12)
and inserted into the NsiI site within areA on
pADPW36 to create pADPW38 (Fig. 1). For its insertion into
areC, genomic DNA from ADPW56 (areC::Km) (Table
1) was digested with XbaI and SacI and ligated
into pUC18, selecting for Apr Kmr
transformants: the plasmid obtained (pADPW45) contained a 6.2-kb insert
with the whole of areR and an areC::Km insert
(Fig. 1). The XbaI-SacI fragment from pADPW45 was
then cloned into pUC18NP to create pADPW46 (Table 1). The Km cassette
in areC was then replaced by the lacZ-Km on a
PstI fragment to create pADPW47 (Fig. 1). In both pADPW38
and pADPW47, lacZ was transcribed in the same direction as
areA and areC, respectively. Both plasmids were
linearized and separately transformed into ADP1 to create ADPW61
(areA::lacZ-Km) and ADPW63
(areC::lacZ-Km), respectively, and integration
into the chromosomes was confirmed by Southern blot analysis (data not
shown).
The Km cassette from pUC4K (26) was inserted into the sole
BglII restriction site in the areR gene of
pADPW71, a HindIII subclone of pADPW45 (Fig. 1), to form
pADPW90 (Fig. 1). It was linearized and transformed into ADP1 to create
ADPW79 (areR::Km), as was confirmed by Southern blot analysis.
Total RNA was prepared from Acinetobacter sp. using an
RNeasy kit (Qiagen). The primer, for primer extension
reactions
(5'-ATCAAGTAATGTCATATAGACCTCGTA-3') complementary to nucleotides on either side of the
areC translational start (boldface), was end labeled with
[
-32P]dATP using T4 polynucleotide kinase and was
annealed to the total RNA at 45°C for 3 h. Reactions were
carried out with avian myeloblastosis virus reverse transcriptase (RT)
(Promega, Madison, Wis.) at 37°C for 1 h. No sequence ladder was
obtained with the same primer, but one was created instead from the
cloning vector M13mp18 (28) using the M13 forward primer.
RT-PCR was carried out as described previously (10) by
using the following primer pairs: across the intergenic regions between areC and areB, forward (primer CBf)
5'-TCAAAGCGCGTGTAATCGAAAAGGTCAAAC-3' and reverse (primer
CBr) 5'-ATGCCCATCTGGATCTCCACCACTGAAGT-3'; for the intergenic
region between areB and areA, forward (primer BAf) 5'-CAGGCGGTGGTGTAAAGTTTGCTCTTGAAT-3' and reverse
(primer BAr) 5'-ATTGCCCCCTGCGCTGTCTCCTG-3'. Sequence
determinations and analysis were performed as described previously
(9, 10).
Induction of the areCBA genes in ADP1.
Induced
AreA, AreB, and AreC activities were found in extracts of cells grown
on all three pathway substrates that were compared with uninduced
(succinate-grown) cells (Table 2),
indicating that growth on each induces all three are genes.
Induction of areA and areC expression by
are operon substrates in strains ADPW61 and
ADPW63.
-Galactosidase activities of whole cells of
ADPW61 (areA::lacZ-Km) and ADPW63
(areC::lacZ-Km) cultures were determined after growth to late log phase on succinate in the presence of aromatic inducers (15).
Benzyl acetate, benzyl alcohol, and benzaldehyde induced transcription
of -galactosidase in ADPW61 and ADPW63 (Table
3), and in the latter, the activities
were approximately 8- to 10-fold higher than in ADPW61. Benzyl acetate,
2-hydroxybenzyl (salicyl) acetate, and 4-hydroxybenzyl acetate were
equally effective as inducers, but the level of induction decreased as
the length of the aliphatic chain of benzyl esters increased from
acetate through propionate to butyrate (Table 3).
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TABLE 3.
Induction by benzyl acetate and its metabolites of
-galactosidase activity expressed from
are::lacZ chromosomal fusions
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The transcription initiation site of the are
genes.
Primer extension reactions using RNA purified from induced
ADP1 cells grown on either benzyl acetate or benzyl alcohol (Fig. 3) showed two products. The strongest
corresponded to 97 bases upstream of the areC ATG, showing
the transcription start site at an A residue at position +1 (Fig.
4), but there was also a second, weaker
extension product corresponding to the adjacent T residue at position
1. No primer extension products were found in succinate-grown cells.
Upstream of the start of transcription is a 12, 24 consensus
element for a 54 promoter binding site. The genetic
organization of the areR-to-areC intragenic
region, including the start codon and the putative ribosome binding
site of areC, can be deduced (Fig. 4).
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FIG. 3.
Primer extension of mRNA from Acinetobacter
sp. strain ADP1. The experiment was performed with total RNA and a
primer which overlaps the putative start codon of areC.
Lanes A, C, G, and T show the respective products from M13mp18 that
were sequenced using the M13 forward primer to size the extension
products. The bases on the left are from the corresponding M13
sequence. Lanes E, F, and H represent the signal obtained from the
experiment using 10 µg of total RNA from cells of ADP1 grown with
benzyl acetate, benzyl alcohol, or succinate, respectively, as the sole
carbon sources. The locations corresponding to both transcriptional
starts are designated by the arrow and are positions 112 and 111 from
the 5' end of the universal primer. The corresponding bases on the ADP1
sequence are shown in Fig. 4.
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FIG. 4.
Regulatory sequences upstream of areC. The
start codon of areC is indicated, and the putative ribosome
binding site (Shine-Dalgarno) of areC is indicated above the
sequence (RBS). The nucleotides corresponding to both primer extension
signals (Fig. 3) are indicated by the double-headed arrow with the
strongest numbered as the +1 site. The putative 12, 24 promoter
elements are indicated. Arrows below the sequence mark an inverted
repeat that is hypothesized to act as the binding site for the
regulator protein. Dashed arrows above the sequence mark a direct
repeat.
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RT-PCR of induced ADP1 total RNA.
RT-PCR conducted on RNA that
was purified from induced ADP1 cells amplified products across the
boundaries between areC to areB (953 bp) and
areB to areA (946 bp), which had both the
expected sizes and restriction sites in the expected positions (Fig.
5). No RT-PCR products using primers
whose products would span the areR-to-areC and
areA-to-salD intergenic regions were obtained from the same RNA preparations, indicating the absence of transcription across these regions (data not shown).
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FIG. 5.
Agarose gel electrophoresis of RT-PCR products amplified
by primers from ADP1 grown on benzyl acetate and benzyl alcohol. The
positions of the primers for spanning the areAB intergenic
region (BAr, BAf) and the areCB intragenic region (CBr, CBf)
are shown relative to the gene organization of areCBA. The
values for molecular size markers (in base pairs) in lanes S
(HyperLadder I; Bioline, London, United Kingdom) are indicated on the
right side of the gel. Lanes: 1, areCB, benzyl acetate-grown
cells (expected size, 953 bp); 2, areCB, benzyl
acetate-grown cells digested with SacI (640 and 313 bp); 3, areCB, benzyl alcohol-grown cells (expected size, 953 bp);
4, areCB, benzyl alcohol-grown cells digested with
SacI (640 and 313 bp); 5, areBA, benzyl
acetate-grown cells (expected size, 946 bp); 6, areBA,
benzyl acetate-grown cells digested with AccI (631 and 315 bp); 7, areBA, benzyl alcohol-grown cells (expected size,
946 bp); 8, areBA, benzyl alcohol-grown cells digested with
AccI (631 and 315 bp). No detectable products were obtained
in control reactions with each pair of primers, from which RT had been
omitted, or in reactions carried out on succinate-grown cells (data not
shown).
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Analysis of ADPW79 (areR::Km) growth phenotype.
Growth of ADPW79 on minimal medium plates containing benzyl acetate,
benzyl alcohol, and benzaldehyde was drastically reduced, taking 2 to 3 days to grow to the same colony size that ADP1 attained overnight.
Thus, as with the areCBA gene disruptions (9),
insertional inactivation of the gene did not result in a complete loss
of ability to grow on the substrates and is probably due to low levels of other enzymes with overlapping substrate specificities
(9).
Induction of areCBA in ADPW79 and ACN274.
By
comparison with ADP1, AreA, -B, and -C in extracts of ADPW79
(areR::Km) grown on minimal media containing succinate plus benzyl alcohol (Table 2) exhibited no induced activities. In the
rpoN mutant ACN274, which has the same reduced growth on the Are substrates as does ADPW79, the activity levels of AreA and AreC
were partially elevated by growth on succinate plus benzyl alcohol
above those in uninduced ADP1 but were still significantly below those
in induced cells of ADP1.
All the evidence presented indicates that areCBA is an
operon which is coordinately induced by AreR. The three genes are
transcribed in the same direction, with only short intragenic
regions. At the mRNA level, we have shown by RT-PCR that transcription
is continuous across both intragenic regions areC to
areB and areB to areA but that
continuity of transcription does not extend to the two flanking genes,
areR and salD. The only hint of an additional regulatory element is the presence of a small, inverted repeat within
the areB-to-areA intragenic region, which might
act as a partial transcription terminator and could account for the
difference in activities beween ADPW61 and ADPW63. Downstream, 11 bp
from the stop codon of areA, is a 17-bp perfect
inverted repeat sequence, 5'-AATTAAAAAGGTTCTTAATAAGAACCTTTTTAATT-3',
which is the likely candidate to be a transcriptional terminator
for the operon.
Biochemical analysis also points to AreA, -B, and -C being coordinately
induced. We demonstrated that AreB and AreC activities were induced by
growth of ADP1 on benzyl acetate and benzyl alcohol (9)
and have now extended the assays of ADP1 to include the esterase
(AreA). Growth on benzyl acetate, benzyl alcohol, or benzaldehyde
causes induction of all three enzymes (Table 2). This indicates
coordinate rather than sequential expression, since in the case of
growth on benzyl alcohol and benzaldehyde, the esterase AreA (and also
the alcohol dehydrogenase AreB for growth on benzaldehyde) is not
required for growth and yet is induced. It cannot be deduced from these
data for ADP1 which compound or compounds can induce, since active
metabolism is occurring. However, the use of a promoterless
lacZ as a reporter gene to monitor are gene
expression clarifies this (Table 3), since the lacZ-Km
cassette has its two genes in opposite orientations with a central
transcriptional terminator and therefore exerts a polar effect on
downstream genes (12). With lacZ inserted into
areA (ADPW61), -galactosidase activity was induced by
benzyl acetate, confirming that benzyl acetate must be an inducer,
since it cannot be metabolized because of the areA
insertional inactivation. Additionally in ADPW63, with lacZ
in areC, thus blocking transcription of all three genes, -galactosidase was induced by all three aromatic metabolites, indicating nonspecificity in the control of expression. In addition, a
variety of esters with modifications in the aromatic alcohol moiety (2- and 4-hydroxybenzyl acetates) and in the alkanoic acid moieties (benzyl
propionate and butyrate), all of which act as substrates, also
induce -galactosidase in both ADPW61 and -63.
The regulator protein for areCBA appears to be AreR.
Upstream, 74 bp from the 12, 24 promoter is an 18-bp inverted
repeat with only two mismatches. Each half of the inverted repeat
contains two direct repeats of 7 bp (Fig. 4), which could provide the
binding site for a regulator protein, since an inverted repeat sequence has also been postulated to act as the regulator binding site in the
related DmpR system (22). It could also serve as a
transcription terminator for areR, since it is located only
10 bp downstream of its termination codon.
The sequence of areR has all the characteristics of the
54-dependent NtrC/XylR family of regulatory proteins
(16, 18, 21). The two most homologous proteins in the
databanks are the AcoR proteins from Clostridium magnum
(13) and Pseudomonas putida (GenBank accession
no. CAA72019). Alignment of amino acid sequences of AreR with sequences
of these proteins (data not shown), as well as with the two related
regulators of aromatic catabolism in Pseudomonas, DmpR
(24) and XylR (8), shows the three domains characteristic of the bacterial enhancer binding protein family (16, 18). The amino-terminal A domain, which is responsive to the inducers (23), is the least conserved and the most
variable in length, but the sequence from residues 159 and 174 of AreR (PVFNGQGKILGALDIT) is completely conserved between AreR and
both AcoR proteins. The central C domain, carrying the ATPase
activity, is well conserved between the five aligned sequences,
and the lengths of the C domains of the genes are very similar.
In addition to the sequence analysis implicating AreR as the regulator
of areCBA, we have confirmed its physiological role by
insertion of a Km cassette into areR. This not only
drastically reduces the growth rate on the are substrates
but also knocks out the ability of benzyl alcohol to induce all three
Are protein activities (Table 2). Induction of the Are enzymes is also
much reduced in an rpoN mutant of ADP1 lacking the
54 subunit of RNA polymerase, completing the circle of
evidence implicating the regulatory protein, promoter, and sigma factor in the induction of areCBA.
| |
ACKNOWLEDGMENTS |
This research was funded by a BBSRC research grant (5/P12776).
We thank Helen Wing, University of Birmingham, Birmingham, United
Kingdom, for help with the primer extension experiment.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: School of
Biological Sciences, University of Wales Bangor, Bangor, Gwynedd LL57
2UW, Wales, United Kingdom. Phone: (44) 1248 382363. Fax: (44) 1248 370731. E-mail: P.A.Williams{at}bangor.ac.uk.
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REFERENCES |
| 1.
|
Altschul, S. F.,
W. Gish,
W. Miller,
E. W. Myers, and D. J. Lipman.
1990.
Basic local alignment search tool.
J. Mol. Biol.
215:403-410[CrossRef][Medline].
|
| 2.
|
Ausubel, F. M.,
R. Brent,
R. E. Kingston,
D. E. Moore,
J. G. Seidman,
J. A. Smith, and K. Struhl (ed.).
1987.
Current protocols in molecular biology.
John Wiley & Sons, Inc., New York, N.Y.
|
| 3.
|
Bauchop, T., and S. R. Elsden.
1960.
The growth of microorganisms in relation to energy supply.
J. Gen. Microbiol.
23:457-469[Medline].
|
| 4.
|
Buck, M., and W. Cannon.
1992.
Specific binding of the transcriptional factor sigma-54 to promoter DNA.
Nature
358:422-424[CrossRef][Medline].
|
| 5.
|
Collier, L. S.,
G. L. Gaines III, and E. L. Neidle.
1998.
Regulation of benzoate degradation in Acinetobacter sp. strain ADP1 by BenM, a LysR-type transcriptional activator.
J. Bacteriol.
180:2493-2501[Abstract/Free Full Text].
|
| 6.
|
Collier, L. S.,
N. N. Nichols, and E. L. Neidle.
1997.
benK encodes a hydrophobic permease-like protein involved in benzoate degradation by Acinetobacter sp. strain ADP1.
J. Bacteriol.
179:5943-5946[Abstract/Free Full Text].
|
| 7.
|
Harwood, C. S., and R. E. Parales.
1996.
The -ketoadipate pathway and the biology of self-identity.
Annu. Rev. Microbiol.
50:553-590[CrossRef][Medline].
|
| 8.
|
Inouye, S.,
A. Nakazawa, and T. Nakazawa.
1988.
Nucleotide sequence of the regulatory gene xylR of the TOL plasmid from Pseudomonas putida.
Gene
66:301-306[CrossRef][Medline].
|
| 9.
|
Jones, R. M.,
L. S. Collier,
E. L. Neidle, and P. A. Williams.
1999.
areABC genes determine the catabolism of aryl esters in Acinetobacter sp. strain ADP1.
J. Bacteriol.
181:4568-4575[Abstract/Free Full Text].
|
| 10.
|
Jones, R. M.,
V. Pagmantidis, and P. A. Williams.
2000.
sal genes determining the catabolism of salicylate esters are part of a supraoperonic cluster of catabolic genes in Acinetobacter sp. strain ADP1.
J. Bacteriol.
182:2018-2025[Abstract/Free Full Text].
|
| 11.
|
Juni, E., and A. Janik.
1969.
Transformation of Acinetobacter calcoaceticus (Bacterium anitratum).
J. Bacteriol.
98:281-288[Abstract/Free Full Text].
|
| 12.
|
Kokotek, W., and W. Lotz.
1989.
Construction of a lacZ-kanamycin-resistance cassette, useful for site-directed mutagenesis and as a promoter probe.
Gene
84:467-471[CrossRef][Medline].
|
| 13.
|
Krüger, N.,
F. B. Oppermann,
H. Lorenzl, and A. Steinbüchel.
1994.
Biochemical and molecular characterization of the Clostridium magnum acetoin dehydrogenase enzyme system.
J. Bacteriol.
176:3614-3630[Abstract/Free Full Text].
|
| 14.
|
Merrick, M. J.
1993.
In a class of its own the RNA polymerase sigma factor sigma 54 (sigma N).
Mol. Microbiol.
5:903-909.
|
| 15.
|
Miller, J. H.
1972.
Experiments in molecular genetics.
Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
|
| 16.
|
Morett, E., and L. Segovia.
1993.
The 54 bacterial enhancer-binding protein family: mechanism of action and phylogenetic relationship of their functional domains.
J. Bacteriol.
175:6067-6074[Free Full Text].
|
| 17.
|
Neidle, E. L.,
M. K. Shapiro, and L. N. Ornston.
1987.
Cloning and expression in Escherichia coli of Acinetobacter calcoaceticus genes for benzoate degradation.
J. Bacteriol.
169:5496-5503[Abstract/Free Full Text].
|
| 18.
|
North, A. K.,
K. E. Klose,
K. M. Steadman, and S. Kustu.
1993.
Prokaryotic enhancer-binding proteins reflect eukaryote-like modularity: the puzzle of nitrogen regulatory protein C.
J. Bacteriol.
175:4267-4273[Free Full Text].
|
| 19.
|
Ornston, L. N., and E. L. Neidle.
1991.
Evolution of genes for the -ketoadipate pathway in Acinetobacter calcoaceticus, p. 201-237.
In
K. Towner, E. Bergogne-Berezin, and C. A. Fewson (ed.), The biology of Acinetobacter. Plenum Press, New York, N.Y.
|
| 20.
|
Sambrook, J.,
E. F. Fritsch, and T. Maniatis.
1989.
Molecular cloning: a laboratory manual, 2nd ed.
Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
|
| 21.
|
Shingler, V.
1996.
Signal sensing by sigma54-dependent regulators: derepression as a control mechanism.
Mol. Microbiol.
19:409-416[CrossRef][Medline].
|
| 22.
|
Shingler, V.,
M. Bartilson, and T. Moore.
1993.
Cloning and nucleotide sequence of the gene encoding the positive regulator (DmpR) of the phenol catabolic pathway encoded by pVI150 and identification of DmpR as a member of the NtrC family of transcriptional activators.
J. Bacteriol.
175:1596-1604[Abstract/Free Full Text].
|
| 23.
|
Shingler, V., and T. Moore.
1994.
Sensing of aromatic compounds by the DmpR transcriptional activator of phenol-catabolizing Pseudomonas sp. strain CF600.
J. Bacteriol.
176:1555-1560[Abstract/Free Full Text].
|
| 24.
|
Shingler, V.,
J. Powlowski, and U. Marklund.
1992.
Nucleotide sequence and functional analysis of the complete phenol/3,4-dimethylphenol catabolic pathway of Pseudomonas sp. strain CF600.
J. Bacteriol.
174:711-724[Abstract/Free Full Text].
|
| 25.
|
Thompson, J. D.,
D. G. Higgins, and T. J. Gibson.
1994.
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weights, position-specific gap penalties and weight matrix choice.
Nucleic Acids Res.
22:4673-4680[Abstract/Free Full Text].
|
| 26.
|
Vieira, J., and J. Messing.
1982.
The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers.
Gene
19:259-268[CrossRef][Medline].
|
| 27.
|
Williams, P. A.,
L. M. Shaw,
C. W. Pitt, and M. Vrecl.
1997.
xylUW, two genes at the start of the upper pathway operon of TOL plasmid pWWO, appear to play no essential part in determining its catabolic phenotype.
Microbiology
143:101-107[Abstract].
|
| 28.
|
Yanisch-Perron, C.,
J. Vieira, and J. Messing.
1985.
Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
Gene
33:103-119[CrossRef][Medline].
|
Journal of Bacteriology, January 2001, p. 405-409, Vol. 183, No. 1
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.1.405-409.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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