1 Department of Biological Sciences, University of Idaho, Moscow, ID 83844-3051, USA
2 Fakultät für Biologie, Lehrstuhl für Genetik, Universität Bielefeld, Postfach 100131, D-33501 Bielefeld, Germany
Correspondence
E. M. Top
evatop{at}uidaho.edu
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|
Even though IncP-1 plasmids are infectiously transmitted with high rates, it has been assumed that horizontal transfer is not sufficient for plasmids to be maintained as genetic parasites, given the burden they present to their host, so that they need to carry at least intermittently advantageous traits to be maintained in bacterial populations (Bergstrom et al., 2000). This hypothesis is supported by the fact that so-called cryptic plasmids of the IncP-1 group, comprised solely of genes for replication, stable inheritance, and horizontal transfer, have not been found so far. All known IncP-1 plasmids have, instead, large regions with acquired genes encoding various resistance or degradation traits, which occasionally might augment the fitness of the bacterial host. One of the insertion regions is located near the origin of replication oriV, separating it from the replication gene trfA (Smith et al., 1993
). The other insertion regions are downstream of traC and, in pB4 only, downstream of upf54.4. Here we present the first complete sequence of two promiscuous IncP-1
plasmids that have no insertions in the oriV region and no remnants of deleted transposable elements. Presumably they have recently evolved from a cryptic ancestor. Sequence comparison with the other sequenced IncP-1
plasmids shows evidence that R751, pB10, pJP4, pADP1 and pUO1 also descended from such a cryptic ancestor.
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|
Standard DNA techniques.
Plasmid DNA from the plasmid-containing E. coli DH5 mcr derivatives was isolated with the Nucleobond Kit PC100 on AX100 columns (Macherey-Nagel) according to the protocol supplied by the manufacturer. Recombinant pUC19 derivatives were isolated using the QIAprep Spin Miniprep Kit (Qiagen) according to the manufacturer's instructions. DNA was extracted from agarose gels with the Sephaglas BandPrep Kit (Amersham Pharmacia Biotech) and purified on Sephacryl MicroSpin S-400 HR columns (Amersham Pharmacia Biotech). Restriction enzyme digestion, agarose gel electrophoresis, DNA cloning and transformation of E. coli DH5
mcr was carried out according to Sambrook et al. (1989)
.
Construction of a shotgun library and DNA sequencing of pB2 and pB3.
Purified plasmid DNA was randomly fragmented and the 1·01·5 kb size fraction was cloned into the sequencing vector pUC19 (Qiagen). Plasmid DNA was prepared from E. coli DH10B shotgun clones with the BioRobot 9600 (Qiagen). Standard shotgun sequencing reactions using the dye-terminator were separated on an ABI 3700 (Applied Biosystems) DNA sequencer, resulting in 825 and 892 sequencing reads with 589 and 578 bases mean sequence length for pB2 and pB3, respectively. Sequencing reads were assembled using the phred/phrap assembly (Ewing et al., 1998). Gap closure and polishing of the sequence was done by primer walking using the dye-terminator chemistry on an ABI 377 sequencer (IIT Biotech). A 4·6 kb EcoRI restriction fragment of pB2 was cloned and sequenced by primer walking to verify the duplication of tetA(C)tetRIS26.
DNA sequence analysis and annotation.
Annotation of the finished sequence was done by using the GenDB (version 2.0) annotation tool (Meyer et al., 2003), as recently described by Tauch et al. (2003b)
. Multiple sequence alignments and motif searches were done by using the VectorNTI Suite 9 (Informax). Phylogenetic analyses were done with DNAmlk 3.5 (J. Felsenstein) incorporated into BioEdit (Hall, 1999
). The tree topologies were not affected by constraints of the underlying evolutionary model as confirmed by maximum-likelihood analysis without molecular clock (default parameters, RP4 as outgroup) using PAUP* (Swofford, 1991
).
![]() |
RESULTS AND DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|
Sequence annotation of pB3 revealed the typical structure of an IncP-1 plasmid backbone (Fig. 1
), as described for R751 (Thorsted et al., 1998
): the regions Tra1 (tra) and Tra2 (trb) with genes required for conjugative transfer and the origin of conjugative replication oriT, the central control region (Ctl) harbouring genes for regulation and stable inheritance, the replication genes trfA and ssb, and the origin of vegetative replication oriV. The partitioning gene parA is located downstream of upf31.0. The encoded parA gene product is homologous to ParA of the IncP-1
plasmid pB4 (Tauch et al., 2003b
) (94 % identity) and to ParA of the IncP-1
plasmid RP4 (Pansegrau et al., 1994
) (75 % identity), belongs to the PinR family of site-specific recombinases (COG1961) and possesses the N-terminal domain of resolvases (Pfam00239). Plasmid pB3 contains an intact parA gene, whereas the 5' part of parA has been deleted in pB4 and R751 (Thorsted et al., 1998
), and the entire gene is absent in the IncP-1
plasmids pB10 (Schlüter et al., 2003
), pUO1 (Sota et al., 2003
), pJP4 (Trefault et al., 2004
) and pADP1 (Martinez et al., 2001
). This ParA protein encoded on pB3 might enhance stable inheritance of the plasmid by resolution of multimers.
|
Plasmid pB3 diverged early from IncP-1 plasmids similar to R751
The availability of seven complete sequences of IncP-1 plasmids provides a large dataset to infer a phylogeny of this plasmid group. Maximum-likelihood trees of different parts of the backbone were constructed in order to see whether they show a common phylogeny or whether recombination events affected the evolutionary histories. The phylogenetic trees calculated on the basis of the conserved IncP-1 backbone regions Tra1 (traCtraM, 13·8 kb in pB3), Tra2 (trbAtrbP, 13·6 kb in pB3) and trfAssb (1·6 kb in pB3) have basically identical topologies (Fig. 2). Plasmid RP4 represents the distant IncP-1
group, and the IncP-1
plasmid pB4 diverged early from pB3 and the other four plasmids, which form the R751 group (plasmids R751, pUO1, pADP1 and pB10). R751 is the best-studied IncP-1
plasmid, and the other three plasmid backbones show on average more than 95 % identity to R751. Several other resistance and degradative plasmids belong to this group as well, such as R906, R772 and pTSA (Smith & Thomas, 1987
; Schlüter et al., 2003
; Tralau et al., 2001
). Plasmid pB3 is clearly separated from this R751 group in these three backbone regions. The tree of the Ctl region (klcAupf54·4, 8·3 kb in pB3) seems to be different, because pB10 appears to be more related to pB4. This is due to the recently described recombination of part of the central control region between incC2 and oriV of pB10 with a pB4-like plasmid (Schlüter et al., 2003
). This is made clear by the change in tree topology of the adjacent genes korB and incC2. The tree of korB (and kfrA, data not shown) supports the phylogeny inferred from the other backbone regions, while in the tree of incC2 (and klcA, data not shown) pB10 clusters with pB4. The same is true for the recently sequenced catabolic plasmid pJP4 (Trefault et al., 2004
), as its backbone is nearly identical to that of pB10 (only 5 base changes in 39 030 bp, without considering columns with gaps in the alignment). In conclusion, the plasmid pB3, which lacks an insertion in the oriV region, and the R751 group of plasmids (R751, pUO1, pADP1, pJP4 and pB10), which all have transposable elements inserted in proximity to oriV, seem to be derived from a common ancestor.
|
The borders of acquired genetic elements in the completely sequenced IncP-1 plasmids were identified based on similarities to transposable elements, inverted repeats, target-site duplications and adjacent sequences common to other IncP-1 plasmids. The remaining backbone sequences were aligned to infer the structure of a common ancestor in the insertion regions. The 1·5 kb oriV region between trfA and klcA of pB3 is contiguous, as predicted for an ancestral IncP-1 replication system, but unlike all known naturally occurring IncP-1 plasmids (Smith et al., 1993). It harbours all the typical sequence motifs of protein binding sites: A/T- and G/C-rich regions of the oriV, palindromic repeats and the transcriptional terminator downstream of trfA (Fig. 3
a). The last two features are missing in RP4. Plasmids pB10, pJP4 and pB4 only have two TrfA-binding sites left of the DnaA-binding site, as shown in Fig. 3a
. In fact, this region (Fig. 3a
, up to the red bracket in pB10) seems to be the left-hand end of the fragment in pB10, which presumably entered by homologous recombination with a pB4-like plasmid (Schlüter et al., 2003
). Both plasmids pB10 and pJP4 share a recombined region similar to pB4 between oriV and incC2, and their backbone sequences in the oriV region are identical, except for a 388 bp deletion adjacent to the insertion site in pJP4. In pUO1 and pADP1, deletions between short direct repeats have removed the fourth palindromic repeat. In plasmid pB3, there is no evidence for the deletion of an accessory element which might have previously been inserted in the oriV region. All the other plasmids have mobile genetic elements, or remnants of them, inserted at various positions. Thus, in this region, each of these plasmids appears to originate from an ancestor like pB3.
|
The only acquired mobile genetic element in pB3 was found between the transcriptional terminator and the palindromic repeats downstream of traC and upstream of parA, i.e. between the trb and the tra region (Fig. 4). The 5 bp target site duplication of the insertion and the 26 bp inverted repeats of the mobile genetic element are still intact (Fig. 4
, lower part), indicating that the insertion occurred recently into an ancestral plasmid without any accessory genes. The insertion site is identical to that of the Tn402-like mer transposon Tn4672 in pUO1. The mobile genetic elements of R751, pADP1 and the plasmids from the same wastewater plant, pB10 and pB4, have different insertion sites downstream of traC (Fig. 4
). Interestingly, plasmid pJP4 has no insertion downstream of traC, and its backbone is completely homologous to that of pB3 in this region. The inverted repeats flanking the composite mobile genetic element in pB3 differ from those in R751 and pUO1 by two mismatches (Fig. 4
, lower part). In all plasmids analysed, except pB3, the left-hand inverted repeats and part of the backbone to the left of the insertion sites were deleted to various extents. In contrast, the backbone to the right of the insertion sites remained intact. The genetic mechanism responsible for such asymmetric deletions is not clear.
|
The pB3 genetic load downstream of the conjugative transfer gene traC contains three distinct mobile genetic elements
A 14·4 kb mobile genetic element flanked by the 5 bp target duplication and the 26 bp inverted repeats is inserted between traC and parA (Fig. 5). It contains a gene for a new class D
-lactamase (blaNPS-2), a tetracycline resistance module tetA(C)tetR, which is flanked by copies of IS26, and a class 1 integron terminated by an insertion of IS6100. The blaNPS-2 gene upstream of parA encodes a
-lactamase that is, respectively, 72 % and 71 % identical to the LCR-1
-lactamase of Pseudomonas aeruginosa (Couture et al., 1992
) and the NPS-1
-lactamase of plasmid pB4 from the same wastewater treatment plant (Tauch et al., 2003b
; Pai & Jacoby, 2001
), and thus represents a new variant of this enzyme type. The NPS-2
-lactamase belongs to class D (COG2602), which also includes LCR-1 of P. aeruginosa and NPS-1 encoded by pB4 (Tauch et al., 2003b
). The resolvase gene tniC located downstream of blaNPS-2 is 98 % identical to tniC of transposon Tn402/Tn5090 on R751 (Radström et al., 1994
). As described for ParA, the tniC gene product also is a member of the site-specific recombinase family (COG1961 and Pfam00239). The tniC gene might be regarded as a relict of the Tn402/Tn5090-specific transposition module, which originally consisted of the genes tniC, tniQ, tniB and tniA (Radström et al., 1994
). The organization of the pB3 parAblaNPS-2tniC segment is reminiscent of the corresponding region on plasmid pB4, with the difference that pB4 parA has been deleted and the blaNPS-1 gene has inserted downstream of tniC on pB4. Apparently, the parAtniC intergenic region contains a preferred site for insertion of cassette-like elements containing
-lactamase genes.
|
The class 1 integron on pB3 possesses two resistance gene cassettes: cmlA1 for a chloramphenicol efflux protein and aadA2 encoding a streptomycin/spectinomycin adenylyltransferase. The integron-specific 3' segment consists of the genes qacE1 (small multidrug exporter protein), sul1 (dihydropteroate synthase), orf5 (putative acetyltransferase) and orf6 (conserved hypothetical protein), and is terminated by the insertion of IS6100. IS6100 is flanked by an additional internal copy of the class 1 integron outer end (123 bp IRt end), whereas, on the opposite side, only the 25 bp IRt motif is present. The pB3 integron 3'-segment variant including a terminal IS6100 copy has been frequently found and has been described in detail for the R plasmids pCG4 and pTET3 of Corynebacterium glutamicum (Tauch et al., 2002
, 2003a
), the IncU R plasmid pRAS1 of the fish pathogen Aeromonas salmonicida (Sorum et al., 2003
), Tn2521In33 inserted in the chromosome of P. aeruginosa Dalgleish (Partridge et al., 2002
), plasmid R1033 Tn1696In4 of P. aeruginosa (Partridge et al., 2001
), the multidrug resistance genomic island 1 of Salmonella enterica serovar Typhimurium (Boyd et al., 2001
) and the mobile genome island pKLC102 of P. aeruginosa C (Klockgether et al., 2004
), demonstrating the wide distribution of this integron derivative. Although the pB3 integron does not possess a functional transposition module, the element most probably entered the plasmid by transposition into the resolution site upstream of the resolvase gene tniC. The integron insertion site is flanked by 5 bp direct repeats representing the target-site duplication (GGACT). The tniC upstream regions including the integron target site are almost identical on pB3 and pB4.
In summary, the complex 14·4 kb genetic load region downstream of traC contains five different antibiotic resistance genes, conferring resistance to ampicillin, tetracycline, chloramphenicol, spectinomycin, streptomycin and sulfonamides, which is in agreement with the observed resistance spectrum of E. coli DH5 carrying pB3. The resistance genes are organized on gene cassettes or transposable elements.
Conclusions
Plasmid pB3 and the five sequenced plasmids of the R751 group have a common ancestor. All these plasmids acquired genetic elements in different positions of the oriV region and downstream of traC, with the exception of plasmids pB3 and pJP4, which lack an acquired genetic element in one or other of these two regions. The most straightforward explanation of the evolutionary history of these plasmids is the existence of a common ancestor free of acquired genetic elements. The alternative explanation, that acquired elements were deleted without trace, for example by recombination with another IncP-1 plasmid, and replaced by other elements at a different position each time one of the plasmids evolved, seems to be less likely. Therefore, IncP-1
plasmids without any accessory genes probably exist in microbial communities and occasionally acquire accessory genes by transposition events, resulting in those plasmids that have been found today based on selectable phenotypic traits. Methods such as triparental exogenous plasmid isolation may be a very good approach to capture such IncP-1 plasmids from various habitats, since the selection is based solely on the ability of the plasmid to mobilize a non-conjugative vector, and not on any phenotypic trait (Hill et al., 1992
; Top et al., 1994
). The use of antibiotics selects for plasmids like pB3, which serve as vectors for the spread of accumulated resistance genes between species and habitats, temporarily providing their hosts with a competitive advantage. Similarly, the presence of recalcitrant xenobiotic compounds, such as atrazine and 2,4-D, selects for those same plasmid ancestors to acquire the operons required for degradation of these molecules, thus giving their hosts access to an additional carbon and/or nitrogen source. However, the mobile and promiscuous IncP-1 plasmid backbones alone seem to provide sufficient benefits to a bacterial community for them to be maintained over longer evolutionary times.
![]() |
ACKNOWLEDGEMENTS |
---|
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|
Bingle, L. E. H., Zatyka, M., Manzoor, S. E. & Thomas, C. M. (2003). Co-operative interactions control conjugative transfer of broad host-range plasmid RK2: full effect of minor changes in TrbA operator depends on KorB. Mol Microbiol 49, 10951108.[CrossRef][Medline]
Bouma, J. E. & Lenski, R. E. (1988). Evolution of a bacteria/plasmid association. Nature 335, 351352.[CrossRef][Medline]
Boyd, D., Peters, G. A., Cloeckaert, A., Boumedine, K. S., Chaslus-Dancla, E., Imberechts, H. & Mulvey, M. R. (2001). Complete nucleotide sequence of a 43-kilobase genomic island associated with the multidrug resistance region of Salmonella enterica serovar Typhimurium DT104 and its identification in phage type DT120 and serovar Agona. J Bacteriol 183, 57255732.
Couture, F., Lachapelle, J. & Levesque, R. C. (1992). Phylogeny of LCR-1 and OXA-5 with class A and class D beta-lactamases. Mol Microbiol 6, 16931705.[Medline]
Davison, J. (1999). Genetic exchange between bacteria in the environment. Plasmid 42, 7391.[CrossRef][Medline]
Dröge, M., Pühler, A. & Selbitschka, W. (2000). Phenotypic and molecular characterization of conjugative antibiotic resistance plasmids isolated from bacterial communities of activated sludge. Mol Gen Genet 263, 471482.[CrossRef][Medline]
Enne, V. I., Bennett, P. M., Livermore, D. M. & Hall, L. M. C. (2004). Enhancement of host fitness by the sul2-encoding plasmid p9123 in the absence of selected pressure. J Antimicrob Chemother 53, 958963.
Ewing, B., Hillier, L., Wendl, M. & Green, P. (1998). Basecalling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Res 8, 175185.
Ghigo, J. M. (2001). Natural conjugative plasmids induce bacterial biofilm development. Nature 412, 442445.[CrossRef][Medline]
Grant, S. G. N., Jessee, J., Bloom, F. R. & Hanahan, D. (1990). Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A 87, 46454649.[Abstract]
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41, 9598.
Heuer, H., Krögerrecklenfort, E., Wellington, E. M. H. & 8 other authors (2002). Gentamicin resistance genes in environmental bacteria: prevalence and transfer. FEMS Microbiol Ecol 42, 289302.[CrossRef]
Hill, K. E., Weightman, A. J. & Fry, J. C. (1992). Isolation and screening of plasmids from the epilithon which mobilize recombinant plasmid pD10. Appl Environ Microbiol 58, 12921300.[Abstract]
Klockgether, J., Reva, O., Larbig, K. & Tümmler, B. (2004). Sequence analysis of the mobile genome island pKLC102 of Pseudomonas aeruginosa C. J Bacteriol 186, 518534.
L'Abee-Lund, T. M. & Sorum, H. (2002). A global non-conjugative Tet C plasmid, pRAS3, from Aeromonas salmonicida. Plasmid 47, 172181.[CrossRef][Medline]
Martinez, B., Tomkins, J., Wackett, L. P., Wing, R. & Sadowsky, M. J. (2001). Complete nucleotide sequence and organization of the atrazine catabolic plasmid pADP-1 from Pseudomonas sp. strain ADP. J Bacteriol 183, 56845697.
Meyer, F., Goesmann, A., McHardy, A. C. & 8 other authors (2003). GenDB an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 31, 21872195.
Pai, H. & Jacoby, G. A. (2001). Sequences of the NPS-1 and TLE-1 beta-lactamase genes. Antimicrob Agents Chemother 45, 29472948.
Pansegrau, W., Lanka, E., Barth, P. T. & 14 other authors (1994). Complete nucleotide-sequence of Birmingham IncP-alpha plasmids Compilation and comparative analysis. J Mol Biol 239, 623663.[CrossRef][Medline]
Partridge, S. R., Brown, H. J. & Hall, R. M. (2002). Characterization and movement of the class 1 integron known as Tn2521 and Tn1405. Antimicrob Agents Chemother 46, 12881294.
Partridge, S. R., Recchia, G. D., Stokes, H. W. & Hall, R. M. (2001). Family of class 1 integrons related to In4 from Tn1696. Antimicrob Agents Chemother 45, 30143020.
Radström, P., Skold, O., Swedberg, G., Flensburg, J., Roy, P. H. & Sundström, L. (1994). Transposon Tn5090 of plasmid R751, which carries an integron, is related to Tn7, Mu, and the retroelements. J Bacteriol 176, 32573268.[Abstract]
Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
Schlüter, A., Heuer, H., Szczepanowski, R., Forney, L. J., Thomas, C. M., Pühler, A. & Top, E. M. (2003). The 64 508 bp IncP-1 antibiotic multiresistance plasmid pB10 isolated from a wastewater treatment plant provides evidence for recombination between members of different branches of the IncP-1
group. Microbiology 149, 31393153.[CrossRef][Medline]
Schnabel, E. L. & Jones, A. L. (1999). Distribution of tetracycline resistance genes and transposons among phylloplane bacteria in Michigan apple orchards. Appl Environ Microbiol 65, 48984907.
Sikorski, R. S., Michaub, W., Levin, H. L., Boeke, J. D. & Hieter, P. (1990). Trans-kingdom promiscuity. Nature 345, 581582.[Medline]
Smith, C. A. & Thomas, C. M. (1987). Comparison of the organisation of the genomes of phenotypically diverse plasmids of incompatibility group P: members of the IncP sub-group are closely related. Mol Gen Genet 206, 419427.[Medline]
Smith, C. A., Pinkney, M., Guiney, D. G. & Thomas, C. M. (1993). The ancestral IncP replication system consisted of contiguous oriV and trfA segments as deduced from a comparison of the nucleotide sequences of diverse IncP plasmids. J Gen Microbiol 139, 17611766.[Medline]
Sorum, H., L'Abee-Lund, T. M., Solberg, A. & Wold, A. (2003). Integron-containing IncU R plasmids pRAS1 and pAr-32 from the fish pathogen Aeromonas salmonicida. Antimicrob Agents Chemother 47, 12851290.
Sota, M., Kawasaki, H. & Tsuda, M. (2003). Structure of haloacetate-catabolic IncP-1 plasmid pUO1 and genetic mobility of its residing haloacetate-catabolic transposon. J Bacteriol 185, 67416745.
Swofford, D. L. (1991). PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1. Computer program distributed by the Illinois Natural History Survey, Champaign, Illinois.
Tauch, A., Götker, S., Pühler, A., Kalinowski, J. & Thierbach, G. (2002). The 27·8-kb R-plasmid pTET3 from Corynebacterium glutamicum encodes the aminoglycoside adenyltransferase gene cassette aadA9 and the regulated tetracycline efflux system Tet 33 flanked by active copies of the widespread insertion sequence IS6100. Plasmid 48, 117129.[CrossRef][Medline]
Tauch, A., Pühler, A., Kalinowski, J. & Thierbach, G. (2003a). Plasmids in Corynebacterium glutamicum and their molecular classification by comparative genomics. J Biotechnol 104, 2740.[CrossRef][Medline]
Tauch, A., Schlüter, A., Bischoff, N., Goesmann, A., Meyer, F. & Pühler, A. (2003b). The 79,370-bp conjugative plasmid pB4 consists of an IncP-1 backbone loaded with a chromate resistance transposon, the strAstrB streptomycin resistance gene pair, the oxacillinase gene blaNPS-1, and a tripartite antibiotic efflux system of the resistance-nodulation-division family. Mol Gen Genomics 268, 570584.[Medline]
Thomas, C. M. & Smith, C. A. (1987). Incompatibility group P plasmids: genetics, evolution, and use in genetic manipulation. Annu Rev Microbiol 41, 77101.[CrossRef][Medline]
Thorsted, P. A., Macartney, D. P., Akhtar, P. & 9 other authors (1998). Complete sequence of the IncP plasmid R751: Implications for evolution and organisation of the IncP backbone. J Mol Biol 282, 969990.[CrossRef][Medline]
Top, E. M., Moënne-Loccoz, Y., Pembroke, T. & Thomas, C. M. (2000). Phenotypic traits conferred by plasmids. In The horizontal gene pool, pp. 249286. Edited by C. M. Thomas. Amsterdam: Harwood Academic Publishers.
Top, E., De Smet, I., Mergeay, M. & Verstraete, W. (1994). Exogenous isolation of mobilizing plasmids from polluted soils and sludges. Appl Environ Microbiol 60, 831839.[Abstract]
Top, E., Vanrolleghem, P., Mergeay, M. & Verstraete, W. (1992). Determination of the mechanism of retrotransfer by mechanistic mathematical modeling. J Bacteriol 174, 59535960.[Abstract]
Tralau, T., Cook, A. M. & Ruff, J. (2001). Map of the IncP-1 plasmid pTSA encoding the widespread genes (tsa) for p-toluenesulfonate degradation in Comamonas testosteroni T-2. Appl Environ Microbiol 67, 15081516.
Trefault, N., De la Iglesia, R., Molina, A. M., Manzano, M., Ledger, T., Pérez-Pantoja, D., Sánchez, M. A., Stuardo, M. & González, B. (2004). Genetic organization of the catabolic plasmid pJP4 from Ralstonia eutropha JMP134 (pJP4) reveals mechanisms of adaptation to chloroaromatic pollutants and evolution of specialized chloroaromatic degradation pathways. Environ Microbiol 6, 655668.[CrossRef][Medline]
Trieu-Cuot, P., Carlier, C., Martin, P. & Courvalin, P. (1987). Plasmid transfer by conjugation from Escherichia coli to Gram-positive bacteria. FEMS Microbiol Lett 48, 289294.[CrossRef]
Zatyka, M., Jagura-Burdzy, G. & Thomas, C. M. (1997). Transcriptional and translational control of the genes for the mating pair formation apparatus of promiscuous IncP plasmids. J Bacteriol 179, 72017209.[Abstract]
Received 5 May 2004;
revised 11 August 2004;
accepted 11 August 2004.
HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
INT J SYST EVOL MICROBIOL | MICROBIOLOGY | J GEN VIROL |
J MED MICROBIOL | ALL SGM JOURNALS |