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Journal of Bacteriology, June 2001, p. 3729-3736, Vol. 183, No. 12
Fakultät für Biologie, Lehrstuhl
für Mikrobiologie/Gentechnologie, Universität Bielefeld,
Bielefeld, Germany
Received 18 August 2000/Accepted 28 March 2001
A new insertion element of 1,449 bp with 25-bp perfect terminal
repeats, designated IS1409, was identified in the
chromosome of 4-chlorobenzoate-degrading Arthrobacter
sp. strain TM1 NCIB12013. Upon insertion, IS1409 causes
a target duplication of 8 bp. IS1409 carries only a
single open reading frame of 435 codons encoding the transposase
TnpA. Both TnpA and the overall organization of IS1409
are highly similar to those of some related insertion elements of the
ISL3 group (J. Mahillon and M. Chandler, Microbiol. Mol. Biol. Rev. 62:725-774, 1998). IS1409 was also found in
other 4-chlorobenzoate-degrading Arthrobacter strains
and Micrococcus luteus. Based on IS1409, a series of transposons carrying resistance genes for chloramphenicol and gentamicin were constructed. These transposons were used to demonstrate transposition events in vivo and to mutagenize
Arthrobacter sp. strains.
Insertion elements (IS
elements) are small mobile non-self-replicating DNA regions specifying
only the gene(s) required for their transposition (16).
According to the phylogenetic relationship of the transposases and some
features involved in the transposition (e.g., the inverted repeats
which constitute the ends of most elements, as well as the recognition
sites of the transposase and the target duplication caused by most
elements), they can be grouped in different families (16).
At least for some IS elements, a target-sequence-dependent site
preference has been demonstrated, while members of other families
apparently transpose in a random fashion. They are widespread in
bacteria and contribute to the plasticity of bacterial genomes due to
their transposition ability and to their role as target sites
for homologous recombination, which can give rise to deletions,
inversions, or more complex rearrangements (20). Some
composite transposons derived from IS elements, in addition to the
genes required for transposition, harbor genes encoding resistances to
antibiotics or degradative pathways.
Arthrobacter, a very common soil bacterium, and related
genera like Micrococcus form one of the major branches of
the actinomycetes, the Micrococcaceae
(30). Some Arthrobacter strains are known to
degrade aromatic compounds as well as chlorinated aromatic compounds
such as 4-chlorobenzoate (4-CBA). Hydrolytic dehalogenation of 4-CBA by
Arthrobacter sp. strain SU DSM20407 requires three genes
organized in an operon which maps on plasmid pASU1 (25). The same set of genes is also present in Arthrobacter sp.
strain TM1 (17). In the course of cloning and sequencing
of these genes (unpublished data), we identified an IS element upstream
of the dehalogenase operon in Arthrobacter sp. strain TM1.
So far, only one other IS element in Arthrobacter and the
Micrococcaceae, IS1473 from Arthrobacter
nicotinovorans (which belongs to the IS3 family), has
been described (19). A growing number of genes specifying degradation of aromatic compounds are known to be located on or associated with transposable elements (for recent reviews see references 31 and 41), with the best known
examples being the very large catabolic transposons Tn4651
and Tn4653 on the TOL plasmids of pseudomonads. Thus, it
seems possible that the genes for the hydrolytic dehalogenation of
4-CBA are located on a transposon.
In order to demonstrate that IS1409 is a functional
transposable element, a series of transposons were constructed based on a slightly modified IS1409 and carrying antibiotic
resistance genes. These transposons are the first which can be used for
transposon mutagenesis in Arthrobacter.
Bacterial strains, plasmids, culture media, and antibiotics.
Bacterial strains and plasmids used in this study are listed in Table
1. 4-CBA-degrading strains were grown at
28°C in a minimal medium as described by Seiler (27) at
pH 8.0, supplemented with 1 g of 4-CBA/liter as the only carbon
and energy source and 0.2 ml of trace element solution/liter
(9). All other actinomycetes were grown in NBYE medium (8 g of nutrient broth and 5 g of yeast extract/liter; pH 7.5) at
28°C. Escherichia coli strains were grown in TBY (10 g of
tryptone, 5 g of yeast extract, and 5 g of NaCl/liter; pH
7.5) at 37°C. For growing recombinant E. coli strains
harboring pUC vector derivatives, ampicillin (150 µg/ml) was added to
the medium. For Arthrobacter spp., chloramphenicol (10 µg/ml) or gentamicin (40 µg/ml) was added to the medium after electroporation of pKGT452 derivatives.
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.12.3729-3736.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Isolation and Characterization of IS1409, an
Insertion Element of 4-Chlorobenzoate-Degrading
Arthrobacter sp. Strain TM1, and Development of a System
for Transposon Mutagenesis
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
TABLE 1.
Bacterial strains and plasmids used
DNA isolation, manipulation, and transfer. Plasmid DNA of E. coli was prepared by the alkaline lysis method (22). Plasmid DNA used for sequencing and electroporation was isolated and purified with Qiagen columns as specified by the manufacturer (Qiagen, Hilden, Germany). The endogenous plasmids of Arthrobacter oxidans and Arthrobacter sp. strain SU were isolated from 1-liter cultures grown overnight in half-strength NBYE containing 1 g of 4-CBA/liter by the method of Kieser (13) using 40°C as the lysis temperature. Preparation of total DNA for hybridization was done as described by Hopwood et al. (9). For total DNA preparation, all strains were grown in rich medium overnight. DNA restriction, ligation, and transformation were carried out by standard procedures (22). Isolation of restriction fragments from agarose gels was done with the JETSORB kit as specified by the manufacturer (Genomed, Bad Oeynhausen, Germany).
Electroporation.
Cultures (100 ml) were grown in NBYE to an
optical density at 580 nm of about 0.5. The cells were harvested and
resuspended in 10 ml of ice-cold deionized water containing 10%
glycerol. Lysozyme (100 µl; 4 mg/ml) was added, and the cells were
incubated at 28°C for 30 min. After harvesting, cells were washed
twice with deionized water-10% (vol/vol) glycerol and then
resuspended in 1 to 5 ml of deionized water-10% (vol/vol) glycerol.
For electroporation, 1 µg of DNA was added to 200 µl of pretreated
cells. Electroporation was performed with a Bio-Rad gene pulser
apparatus applying the following parameters: capacity, 25 µF;
voltage, 2.5 kV/cm; resistance, 600 to 800 
, giving a pulse length
of 10 to 13 ms. Cells were mixed immediately with 0.8 ml of SB medium
(10 g of tryptone/liter, 5 g of yeast/liter, 4 g of
NaCl/liter, 0.5 M sorbitol, 20 mM MgCl2, 20 mM
CaCl2 [pH 7.5]) and incubated for 2 h at
28°C before plating on appropriate selective media. Afterwards
colonies were restreaked on NBYE plates containing the appropriate antibiotics.
Southern blot analysis.
The internal 1-kb SstI
fragment of the tnpA gene from pKGT21 was labeled using the
random primed DNA labeling kit (Boehringer Mannheim, Mannheim,
Germany) and used as probe for the transposase gene of
IS1409. A 2.2-kb SphI/BglII fragment
of pKGT452C
was used to detect the cmx gene. pUC13 DNA
labeled with digoxigenin-11-dUTP by nick translation (22)
was used as a probe for integration of the transposon delivery vector.
Digested chromosomal and plasmid DNA samples were separated on 0.7 to
1.0% agarose gels and transferred to nylon membranes (Hybond
[Amersham, Little Chalfont, United Kingdom] or Nytrans [Schleicher & Schuell, Dassel, Germany]) using a vacuum blotter (Vacugene;
Pharmacia). Hybridizations were carried out at 68°C overnight in a
buffer containing 5× SSC (1× SSC is 0.15 M NaCl plus 0.015 M sodium
citrate), 0.02% sodium dodecyl sulfate, 0.1% Na laurylsarcosyl, and
2% blocking reagent (Boehringer Mannheim). The nylon membrane was
washed twice with 0.1× SSC-0.1% sodium dodecyl sulfate at 68°C for
15 min.
DNA sequencing and sequence analysis.
For DNA sequencing,
the dideoxy chain termination method (24) was used with
[
-32P]dATP (3,000 Ci/mmol) employing
Sequenase 2.0 or Taqquence sequencing kits from U.S. Biochemicals
(Cleveland, Ohio) as specified by the manufacturer. For sequence
determination, either subclones of pKGT45 were constructed or primer
walking with synthetic oligonucleotides (obtained from TIB Molbio,
Berlin, Germany, or from Birsner and Grob-Biotech GmbH,
Denzlingen, Germany) was conducted. Oligonucleotides ISC2 (5'-GGA
ACC TCA CCA ACT ACA TAG C-3') and ISN2 (5'-CAT GCA GTT GCG
CCC ACT ACA C-3') were used to determine the sequence of
insertion sites in Tn1409 mutants. The oligonucleotides IS1 to IS6 were used to introduce two base exchanges into the 5' end of
IS1409 in the construction of pKGT452 (IS1, 5'-AAT TCC
GGT ACC ATG GCT CTT CAG AAT TGA GGG TGT-3'; IS2, 5'-AGT GGG
CGC AAC TGC ATG CAG CGC CGA GGG CTA GCG GCG T-3'; IS3,
5'-GAT TCA GAC AAG GTG AGG GCC TCG GGA GAG AAT CAG ATT GTC
TA-3'; IS4, 5'-GAT CTA GAC AAT CTG ATT CTC TCC CGA GGC CCT
CAC CT-3'; IS5, 5'-TGT CTG AAT CAC GCC GCT AGC CCT CGG CGC
TGC ATG CAG T-3'; IS6, 5'-TGC GCC CAC TAC ACC CTC AAT TCT
GAA GAG CCA TGG TAC CGG-3').
Nucleotide sequence accession number. The sequence reported here has been deposited in GenBank under accession no. AF042490.
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Nucleotide sequence of IS1409.
During the
analysis of the nucleotide sequence of the chromosomally borne
4-CBA dehalogenase operon of Arthrobacter sp. strain TM1
(NCIB12013) on a 25-kb Sau3A fragment inserted into
the cosmid pJE258 (pEZ1) (26), an open reading frame (ORF)
with significant identities to those encoding transposases was
detected. A 2.35-kb EcoRV/NruI fragment of pEZ1
was subcloned into the SmaI site of pUC13, resulting in
plasmid pKGT451 (Fig. 1a). The nucleotide sequence of both strands of pKGT451 was completely determined. The
nucleotide sequence and the deduced amino acid sequence are presented
in Fig. 1b. The sequence surrounding the transposase gene was found to
fulfill the criteria required for an IS element. On both sides of this
inserted element a target sequence duplication of 8 nucleotides (nt)
was found and confirmed by comparison with the homologous sequence on
plasmid pASU1 of Arthrobacter sp. strain SU
(25), which lacks the IS element. IS1409 is
1,449 bp long and has perfect terminal inverted repeats of 25 bp. The
GC content of the IS element is 61.8%, which is in agreement with the
GC content of the Arthrobacter host. IS1409 is
inserted about 500 bp upstream of the 4-CBA dehalogenase operon.
|
Homology of TnpA from IS1409 to transposases of
other IS elements.
Database searches with the deduced TnpA
sequence revealed a number of highly similar transposases of bacterial
IS elements, as shown in Table 2. The
most closely related transposases are found in actinomycetes, with the
exception of IS1411 from a phenol-degrading Pseudomonas putida strain (12). For
IS1096, IS31831, and IS1411 there is
very high identity at the DNA level, with 72, 60, and 57% identities,
respectively, observed over nearly the whole length of the transposase
gene (data not shown). The inverted repeats of these IS elements are
also highly conserved (Fig. 2). Based on
the homology to these transposases, the 8-nt duplication, and the
inverted repeats of 25 bp, IS1409 is classified as a member of the ISL3 family (16).
|
|
Distribution of IS1409 among various bacterial
strains.
Hybridization experiments with an internal 1-kb
SstI fragment of IS1409 as a probe against total
or plasmid DNA of various Arthrobacter strains were
conducted under stringent conditions. For this, DNA was digested with
BglII, which does not cut inside the tnpA gene
(Fig. 3). In Arthrobacter sp.
strain TM1, at least eight copies of IS1409 were found,
displaying different signal intensities. The 4-CBA degrading
Arthrobacter sp. strain SU carries two copies, while only
one copy could be identified for the plasmid-cured derivative
Arthrobacter sp. strain SUX (Fig. 3), indicating that in
these strains one copy of IS1409 is carried by plasmid
pASU1. A. oxidans CBS2 DNA gave only one and
Micrococcus luteus DNA gave two positive signals under
stringent conditions. IS1409 was not identified in any of
the other actinomycetes tested (Table 1 and Fig. 3) under stringent
conditions (data not shown for all strains).
|
EcoRI/HindIII.
Construction of resistance transposons from IS1409. To prove that IS1409 located on pKGT451 is a functional IS element, derivatives carrying resistance genes were constructed. As the nucleotide sequence of pKGT451 revealed that there are no unique restriction sites present between the left inverted repeat and the start of the putative transposase gene, the 120 bp at the 5' end of IS1409 up to the BglII site was replaced by six overlapping synthetic oligonucleotides (IS1 through IS6) which carried two nucleotide exchanges so that unique SphI and NheI sites were created. The oligonucleotides were annealed and inserted into EcoRI/BglII-linearized pKGT451, resulting in pKGT452 (Fig. 1b). The changes in the sequence were confirmed by restriction analysis and nucleotide sequence determination.
Then, the chloramphenicol resistance gene cmx, encoding an exporter protein of Tn5564 of Corynebacterium striatum (32), and the gentamicin acetyltransferase gene aacC1 from Tn1696 (40) were inserted into the NheI site of pKGT452. Both orientations were obtained after ligation as confirmed by restriction analysis and partial sequencing. The resulting plasmids were designated pKGT452C
and - (Fig. 4) and pKGT452G and
-, carrying the transposons Tn1409C and - and
Tn1409G and -, respectively, depending on the
orientation of the resistance cassette relative to the tnpA gene. The size of these transposons is about 3.4 kb.
|
Transposon mutagenesis of Arthrobacter sp.
A
mutagenesis was conducted with Arthrobacter sp. strains SU
and SUX by electroporation using covalently closed circular plasmid DNA
of pKGT452C and - and pKGT452G and - isolated from E. coli JM109. Since pUC13 is not able to replicate in
Arthrobacter, all resistant clones should arise by
transposition or recombination with endogenous copies of
IS1409. The average rates of antibiotic-resistant clones
obtained ranged from 2 × 103 to 1 × 104/µg of DNA in independent experiments. For
both pKGT452C and pKGT452G, which contain the resistance gene and
the tnpA gene oriented in the same direction, about twice as
many antibiotic-resistant clones were obtained as for the corresponding
plasmids where transposase and resistance genes were transcribed in
opposite directions. No significant difference in the number of
resistant clones was found between pKGT452C and pKGT452G.
by either
homologous recombination or cointegrate formation had occurred. In
about 10% of the transposon mutants of strain ASU the signal of the endogenous copy of IS1409 was missing, indicating a
recombination event or a more complex rearrangement between the
introduced transposon and the endogenous IS1409 (data not
shown). However, this does not impair the usefulness of
Tn1409 for transposon mutagenesis, especially when a strain
which does not carry IS1409 is used.
|
Sequence analysis of insertion sites of Tn1409 in
Arthrobacter.
Total DNA of some mutants
generated with Tn1409C was isolated and digested with
SphI (one site in Tn1409C 11 bp downstream of
the left inverted repeat), which leaves the cmx gene intact. The digested DNA was hybridized with digoxigenin-labeled probes for
tnpA (a 1-kb SstI fragment from pKGT21), the
cmx gene (a 2.2-kb SphI/BglII fragment
from pKGT452C), and pUC13. The insertion sites from two mutants (A1
and A27) which did not hybridize with pUC13 were subsequently isolated
as SphI fragments giving a signal with the cmx probe.
59 bp upstream of a gene homologous to
branched-chain -keto acid dehydrogenases (5, 28) in
mutant A27. From another mutant Arthrobacter strain, SU A1,
the hybridizing 4.8-kb SphI fragment was cloned in an
analogous procedure (pKGT1000). Preliminary single-stranded sequence
determination revealed the insertion of Tn1409C into an
ORF with homology to the membrane component of ABC transporters
involved in iron uptake (23). However, growth of mutant A1
on iron-limited media was not impaired (data not shown). In addition,
downstream a small ORF without homologs in the database followed by a
third ORF designated tdk, similar to thymidine kinase genes
(33), was found. The putative target duplication in these
mutants confirmed the apparent random transposition, as no preference
for a specific insertion site was detected.
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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In this report we describe a novel IS element, IS1409, found upstream of the 4-CBA dehalogenase operon of Arthrobacter sp. strain TM1. This IS element was found only in members of the Micrococcaceae, in 4-CBA-degrading Arthrobacter strains, and in M. luteus. IS1409 displays typical features of members of the ISL3 family, with the highest similarity to IS elements from other actinomycetes. The high extent of identity to IS1411 from P. putida may indicate horizontal transfer of this element from gram-positive to gram-negative bacteria.
The mode of transposition, whether replicative or conservative, for the members of the ISL3 family is still unknown. The putative resolvase gene occurring in IS1096 of Mycobacterium smegmatis is not necessary for transposition (18). For IS31831 and ISPs1, the formation of excised transposon circles was reported (2, 38). Integration of the delivery plasmid at low frequency, which was also observed for IS31831 (37), could arise either by recombination or cointegrate formation.
The insertion sites of IS1409 and Tn1409 analyzed so far do not indicate a preference for a specific sequence for insertion. However, both ends of the 8-nt target duplication are rich in GC with an AT-rich central region, for example, TCATTGCCC (endogenous copy), GCCAAAAC (mutant A1), and ACGAAAGT (mutant A27). For the transposons derived from IS1096 and IS31831 (18, 37), the same pattern was reported for the insertion sites. This may often lead to insertions within promoter regions in these high-GC gram-positive bacteria; for example, this may have occurred in mutant A27. Such integrations resulting in gene activation and/or inactivation have also been described for pseudomonads (e.g., for IS1411 and ISPs1) (2, 12).
IS1409 was used to construct antibiotic resistance gene transposons after the exchange of two nucleotides in the upstream region of the tnpA gene. The transposition rates of about 103 transpositions/µg of DNA used in electroporation of Arthrobacter are in the same range as those obtained with transposons constructed from IS1096 (3) and IS31831 (37). Since transposition rates strictly depend on the efficiency of transformation, transposon mutagenesis requires optimization of the conditions for electroporation. Also, the extent of methylation of the DNA used may be important (35).
Although the strains used in transposition experiments possess endogenous copies of IS1409, in most cases a transposition of Tn1409 occurred. Only once did we observe integration of the complete delivery plasmid, and in two cases we found indications of rearrangements as the endogenous IS1409 was lost. Both phenomena could arise either by recombination or during transposition.
The construction of transposon Tn1409, which has a high transposition rate and shows no obvious preference for specific insertion sites, now provides a system for transposon mutagenesis for Arthrobacter which may be very useful for genetic investigations in this important actinomycete.
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ACKNOWLEDGMENTS |
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We thank our colleagues J. Eberspächer (University of Stuttgart, Stuttgart, Germany), J. Kalinowski and A. Tauch (University of Bielefeld, Bielefeld, Germany), F. Lingens (University of Stuttgart), and R. Müller (University of Hamburg, Hamburg, Germany) for supplying strains and plasmids. We are also indebted to E.-M. Zellermann for excellent technical assistance.
This work was supported by the Deutsche Forschungsgemeinschaft Ei 140/11-2.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Microbiology/Gene Technology, University of Bielefeld, Universitaetsstr., 33615 Bielefeld, Germany. Phone: 49(0)5211065558. Fax: 49(0)5211066015. E-mail: eichenlaub{at}biologie.uni-bielefeld.de.
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Abstract
Introduction
Materials and Methods
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Discussion
References
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Journal of Bacteriology, June 2001, p. 3729-3736, Vol. 183, No. 12
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.12.3729-3736.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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