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J Bacteriol. Dec 2007; 189(24): 8855–8862.
Published online Oct 12, 2007. doi:  10.1128/JB.01213-07
PMCID: PMC2168638

Cohabitation of Two Different lexA Regulons in Pseudomonas putida[down-pointing small open triangle]


In contrast to the vast majority of the members of the domain Bacteria, several Pseudomonas and Xanthomonas species have two lexA genes, whose products have been shown to recognize different LexA binding motifs, making them an interesting target for studying the interplay between cohabiting LexA regulons in a single species. Here we report an analysis of the genetic composition of the two LexA regulons of Pseudomonas putida KT2440 performed with a genomic microarray. The data obtained indicate that one of the two LexA proteins (LexA1) seems to be in control of the conventional Escherichia coli-like SOS response, while the other LexA protein (LexA2) regulates only its own transcriptional unit, which includes the imuA, imuB, and dnaE2 genes, and a gene (PP_3901) from a resident P. putida prophage. Furthermore, PP_3901 is also regulated by LexA1 and is required for DNA damage-mediated induction of several P. putida resident prophage genes. In silico searches suggested that this marked asymmetry in regulon contents also occurs in other Pseudomonas species with two lexA genes, and the implications of this asymmetry in the evolution of the SOS network are discussed.

Bacterial cells are able to display a range of responses against the wide spectrum of DNA-damaging agents to which they are frequently exposed. Among these, one of the most studied is the SOS response. First described in Escherichia coli (38), the SOS response comprises a network of more than 40 genes involved in DNA repair, error-prone DNA replication, and cell division regulation (10, 16, 19). Typically, SOS genes are negatively regulated by the LexA repressor protein, which in E. coli recognizes specifically a CTGTN8ACAG regulatory motif present in the promoter region of its target genes. This motif, usually called the SOS or LexA box, has been shown to be different in different phyla, such as the gram-positive bacteria or the α-, β-, γ-, and δ-Proteobacteria (22), and has been shown to be monophyletic in some of them (22). Induction of the SOS genes is triggered by activation of the RecA protein after binding to single-stranded DNA fragments generated either by stalling of the replication fork or enzymatic processing of broken DNA ends (33). Activated RecA is able to induce the autocatalytic cleavage of LexA, thus preventing it from binding its target sites and activating the expression of SOS genes (21). Once DNA damage has been properly addressed, the activated RecA concentration drops and newly synthesized LexA is able to bind again to its target sites, thus switching off the coordinated response. It is worth noting that not all LexA-regulated genes are induced at the same level or at the same time. Instead, the timing, duration, and level of the induction may vary significantly among different SOS genes (10, 30).

Even though the SOS response has been thoroughly characterized in several microorganisms, such as E. coli (10), Pseudomonas aeruginosa (9), and the gram-positive organisms Bacillus subtilis (2) and Staphylococcus aureus (8), both of which have an SOS box (GAACN4GTTC) (8, 40) markedly different from that of E. coli (38), recent work has offered a glimpse of the composition of the LexA regulon in several additional bacterial species (20). In contrast to the examples cited above, the genetic composition of the LexA network has been found to vary widely among phyla and even among species belonging to the same class (14, 22). In this respect, it is interesting that although the majority of bacterial genomes sequenced so far have only one or no LexA homologue, duplication of LexA has been reported previously. The δ-proteobacterium Geobacter sulfurreducens, for instance, has two lexA genes whose products recognize the same regulatory motif and which seem to be the result of a recent duplication event (18). In contrast, the two LexA proteins encoded by several Pseudomonas and Xanthomonas species have been shown to recognize markedly different LexA binding motifs (1, 41). In Pseudomonas putida, one of the two LexA proteins (LexA1) recognizes an E. coli-like SOS box (CTGTN8ACAG), while the other LexA protein (LexA2) binds to a manifestly divergent motif (GTACN4GTGC) (1). In Xanthomonas (41), however, while LexA2 recognizes the same motif that P. putida LexA2 does, the LexA1 protein has been shown to bind a motif (TTAGN6TACTA) previously also found in Xylella fastidiosa, which belongs to the same class (6).

Besides the coincidence in LexA binding motifs, the relationship between Xanthomonas and Pseudomonas LexA proteins has been established through comprehensive phylogenetic analyses (13). Interestingly, the results of these studies also indicate that the lexA2 gene is always cotranscribed with three other DNA damage-inducible genes (PP_3117, PP_3118, and PP_3119, designated here, following the recently proposed nomenclature, imuA, imuB, and dnaE2) (13, 17, 20), which make up a cassette that has been shown to be widespread in the domain Bacteria and to be involved in DNA damage-mediated mutagenesis (1, 13, 17). During its evolutionary history, this multiple-gene cassette has undergone a number of reorganizations, with three-gene, two-gene, and completely split cassettes reported in different phyla but always showing apparent regulation by LexA (13). Phylogenetic reconstruction of the cassette history suggests that the reorganization leading to the lexA2-imuA-imuB-dnaE2 gene cassette seen in Xanthomonas and Pseudomonas took place soon before the split of γ- and β-Proteobacteria and was soon followed by duplication of the cassette and its accompanying lexA gene, at a time when the E. coli LexA binding sequence or a closely related motif had probably already evolved (13).

The presence of two different LexA proteins that do not recognize the same binding site is an uncommon feature in the domain Bacteria that can provide clues concerning the evolution of complex regulatory networks like the SOS response, addressing such issues as the behavior of coexisting lexA genes or the evolution of novel LexA binding sequences. For this reason, the aim of the present work was to analyze the genetic composition of the P. putida lexA1 and lexA2 regulons in order to determine the possible relationships and overlaps between both networks. Gene expression patterns in wild-type cells of P. putida with damaged DNA, as well as in lexA1 and lexA2 mutant derivatives, were determined and examined to reveal the extent of the interplay between the networks.


Bacterial strains and growth conditions.

All bacterial strains and plasmids used in this work are listed in Table S1 in the supplementary material. P. putida KT2440 (25) was grown in LB medium (32) at 30°C. The antibiotic concentrations used for each microorganism were the concentrations previously reported (1, 24). All plasmid construction and cloning experiments were performed using E. coli DH5α (32). Plasmid DNA was transformed into competent E. coli cells as described previously (32). All P. putida mutants were constructed by marker exchange using plasmid pUA658 (Gmr) (see Table S1 in the supplementary material) with the gene of interest interrupted by insertion of an ΩKm cassette into a SmaI restriction target generated by inverted PCR using suitable oligonucleotides (see Table S2 in the supplementary material), as described previously (1). The presence of a transcriptional terminator in the ΩKm cassette eliminated the expression of genes downstream of the truncated gene. In all cases, after serial passages, all the mutant derivatives were genetically stable. The growth ratio in LB media and the cell survival after mitomycin C treatment were determined for each of the constructed mutant derivatives, and the values were not different from the values for the isogenic wild-type P. putida KT2440 strain. Likewise, microscope observation of the mutant strains did not reveal any phenotypic changes.

RNA extraction and RT-PCR.

RNA purification was carried out using a TriPure isolation reagent kit (Tri Reagent LS; Molecular Research Center), followed by DNase I treatment (Roche) and purification with RNeasy columns (Qiagen) as described previously (42). Extraction of total DNA was carried out by standard methods (32). Reverse transcription (RT)-PCR analysis of gene expression was performed as reported previously (1) using specific internal oligonucleotide primers for each gene. The RNA concentration of the gene analyzed was always normalized to the concentration of the trpA gene, whose expression is not affected by DNA damage in P. putida, as described for E. coli (10), nor in the P. putida mutant derivatives used in this work (see Tables S3 and S4 in the supplementary material).


LexA1 and LexA2 proteins were purified previously (1). Promoter fragments for electrophoretic mobility shift assays (EMSA) were isolated by PCR from total P. putida DNA, using suitable oligonucleotide primers designed in accordance with their published sequences. The PCR fragments were cloned in a pGEM-T vector and sequenced. DNA probes were prepared by PCR amplification with one of the primers labeled at the 5′ end with digoxigenin and by purifying each product in a 2 to 3% low-melting-point agarose gel. DNA-protein binding reactions were performed as previously described (1), and the mixtures were loaded onto a 6% nondenaturing Tris-glycine polyacrylamide gel that was prerun for 30 min at 10 V cm−1 in 25 mM Tris-HCl (pH 8.5)-250 mM glycine-1 mM EDTA. DNA-protein complexes were separated at 100 V for 90 min, and this was followed by transfer to a Biodine B nylon membrane (Pall Gelman Laboratory). Digoxigenin-labeled DNA-protein complexes were detected using the manufacturer's protocol (Roche). When necessary, either lexA1 or lexA2 promoter fragments, obtained by PCR performed with the suitable oligonucleotides, were used as an unlabeled DNA competitor (1).

Hybridization and processing of microarrays.

A previously described genome-wide oligonucleotide-based DNA microarray for P. putida KT2440 was used (42). Twenty micrograms of total RNA was transformed to cDNA, and after this Cy3 or Cy5 fluorescent dyes (Amersham Biosciences) were coupled to the amino-modified first-strand cDNA. The labeling efficiency was assessed using a NanoDrop ND1000 spectrophotometer (NanoDrop Technologies). Prehybridization and hybridization microarray analyses were performed as described previously (42). Slides were scanned with a ScanArray 4000 fluorescence scanner. For each experiment, three independent RNA extractions were performed, the extracts were pooled to obtain single samples, and each sample was analyzed with at least two microarrays. The statistical analysis was based on an empirical Bayes method implemented in the software package LIMMA for the R-computing environment (www.r-project.org) (37). A gene was considered to be induced when either the ratio of the treated preparation to the nontreated preparation or the ratio of the wild-type preparation to the mutant preparation was greater than 2.0 and the P value was <0.01.

In silico searches for LexA binding sites.

In silico searches for LexA binding sites were performed with Fitom, a general search program for detection of DNA binding sites based on position-specific weight matrices (PSWM) of known sites that implements several reported methods for scoring putative binding sites. Searches were carried out using the information content-averaged Berg-von Hippel heterology index as the scoring function (3, 27, 28, 35). In order to ensure that the results obtained had low false-positive rates and thus were a reasonable, although necessarily abridged, approximation of data for the true regulon, a restrictive threshold (a score better than that of one-half the PSWM sites) was applied to putative binding sites when full genomes were analyzed. A more relaxed threshold (a score better than 85% of the original PSWM sites) was applied to search for LexA binding sites in the promoter regions of genes that had been shown to be LexA regulated in P. putida. Collections of binding sites to construct both PSWM were obtained from previous publications. For LexA1, 23 experimentally verified binding sites from E. coli (15, 23, 29, 31) were used to construct the PSWM, while seven LexA2 binding sites from several Pseudomonas and Xanthomonas species were used to construct the LexA2 PSWM (1, 41). Genomic sequences were all downloaded from the NCBI GenBank repository through its FTP server (ftp.ncbi.nih.gov).

Microarray accession number.

All the array data have been deposited in the Arrayexpress database (http://www.ebi.ac.uk/arrayexpress) under accession number E-MEXP-1187.


Analysis of gene expression in P. putida lexA1 and lexA2 mutant derivatives.

To determine the genetic composition of the LexA1 and LexA2 regulons and their possible overlap, P. putida KT2440 lexA1 and lexA2 mutant derivatives were obtained by marker exchange by inserting a construct in which either lexA1 or lexA2 was interrupted by a ΩKm cassette insertion. Both P. putida mutant derivatives were completely viable and did not have observable phenotypic differences from the wild-type strain. Using a previously described P. putida KT2440 oligonucleotide-based genomic array (42), the gene expression patterns of both mutant strains were compared to that of the wild type before and after treatment of the latter with mitomycin C.

The results of the array experiments, summarized in Fig. Fig.1,1, revealed that the two mutant derivatives and the nontreated wild-type strain had different expression profiles, indicating that different sets of genes were under control of the LexA1 and LexA2 proteins, as inferred from their increased expression in the mutant derivatives. Moreover, for all genes whose expression was different in the nontreated wild-type strain and the mutant derivatives, LexA binding sequences of the corresponding LexA proteins could be located in their promoter regions, suggesting that there was direct regulation by either the LexA1 or LexA2 protein. Microarrays were also used to analyze the effect of mitomycin C on the transcriptome profile of the wild-type strain. As expected, all genes exhibiting increased expression in the mutant derivatives were also induced in the wild-type strain treated with mitomycin C (Fig. (Fig.1),1), confirming their regulation by either LexA1 or LexA2. Data obtained by microarray analysis were confirmed for all the differentially expressed genes by performing quantitative RT-PCR experiments (not shown).

FIG. 1.
Schematic diagram showing P. putida mitomycin C-induced transcriptional units (TUs) and their relationship to either LexA1 or LexA2 protein regulation. All genes shown had an induction factor higher than 2.0-fold in microarray data compared with either ...

As shown in Fig. Fig.1,1, there are 18 transcriptional units under direct control of LexA1, while only 2 transcriptional units are regulated by LexA2. A more detailed analysis of the LexA1 regulon revealed that, as expected, most of the regulated genes are involved in recombination and DNA repair. Furthermore, the LexA1 regulon of P. putida has a significant overlap with the reported LexA regulons of both E. coli and P. aeruginosa (Table (Table1),1), in which there is only one LexA protein that recognizes the same regulatory motif (CTGTN8ACAG) as P. putida LexA1 (9, 16). In contrast, the P. putida LexA2 protein controls only its own transcriptional unit and a gene (PP_3901) that is also regulated by LexA1. To ascertain whether the observed disparity in regulon contents was the general trend in other Pseudomonas species having two LexA proteins, restrictive in silico searches with both regulatory motifs were conducted for several Pseudomonas genomes to gauge the approximate extents of their LexA1 and LexA2 networks.

Comparison of P. putida lexA1 and lexA2 regulons for both experimentally validated lexA networks of E. coli and P. aeruginosa and in silico searches in other Pseudomonas species encoding both LexA proteinsa

The results, summarized in Table Table1,1, suggest that the imbalance in regulon contents between the two LexA proteins is present in other Pseudomonas species and give further credence to previous phylogenetic analyses (13) which suggested that the lexA2 gene arose as a duplication of an early ancestor.

The only gene directly controlled by both LexA proteins belongs to a prophage.

Apart from the 18 transcriptional units regulated by LexA1 and LexA2 shown in Fig. Fig.1,1, there are a number of genes that were induced in the mitomycin C-treated wild-type strain but were not deregulated in either lexA mutant derivative. All these genes correspond to the coding region of a bacteriophage that has previously been described as P. putida KT2440 genomic island 79 of atypical sequences composed of elements annotated with phagelike gene signatures (39), and their DNA damage-mediated induction profile was initially attributed to a LexA-independent pathway, like that seen in many bacteriophages in which activated RecA promotes self-cleavage of the lytic cycle repressors, thus inducing the bacteriophage (34). However, the fact that the only gene upregulated in both lexA1 and lexA2 mutant derivatives (PP_3901) was in the same bacteriophage coding region suggested that some kind of LexA coregulation might cause the observed induction of phage genes. PP_3901 has regulatory motifs for both LexA1 and LexA2 in its promoter region, and the ability of both LexA proteins to specifically bind the PP_3901 promoter was determined by EMSA (Fig. (Fig.2).2). Moreover, a quantitative RT-PCR experiment was performed (Fig. (Fig.3),3), which validated the array data and confirmed not only that PP_3901 is simultaneously and directly regulated by LexA1 and LexA2 but also that the LexA1 protein plays the leading role in the transcriptional control of PP_3901 expression (Fig. (Fig.3).3). BLAST-P searches with the 86-amino-acid protein coding sequence of PP_3901 resulted in significant matches with paralogous proteins in P. putida (PP_2452), in other Pseudomonas species, like P. syringae (PSPPH_2123), and even in the P. aeruginosa F116 bacteriophage (F116928). In all these cases, however, LexA binding sequences corresponding to the LexA1 motif, but not LexA binding sequences corresponding to LexA2, could be identified in the promoter region of the PP_3901 homologues.

FIG. 2.
(A) Structural arrangement of the P. putida PP_3901 gene promoter. LexA1 and LexA2 binding sites and their positions with respect to the ATG translational starting codon are indicated. The bent arrows indicate the positions of the oligonucleotides used ...
FIG. 3.
Relative expression levels of the PP_3901 gene in the P. putida wild-type (Wt) strain and in lexA1 and lexA2 mutant derivatives of this strain. The expression level was measured by quantitative RT-PCR and is the ratio of the relative mRNA concentration ...

To better understand the possible role of PP_3901 in the induction of phage genes and of its coregulation by the two LexA proteins of P. putida, a PP_3901 mutant derivative was constructed after ensuring, through RT-PCR analysis, that PP_3901 was not part of a transcriptional unit and that its inactivation would not result in polar effects on downstream genes (data not shown). As observed for both LexA mutant derivatives, the morphology and growth of the PP_3901 mutant derivative did not differ from the morphology and growth of the wild-type strain (data not shown). Since PP_3901 is in the coding region of a genome-encoded bacteriophage, the expression of two genes from this region (PP_3873 and PP_3894) that had been shown to be DNA damage inducible in the mitomycin C-treated wild-type strain was analyzed by means of quantitative RT-PCR studies in the PP_3901 mutant derivative.

As Fig. Fig.44 shows, the RT-PCR results indicate that neither prophage gene was induced by mitomycin C treatment in the PP_3901 derivative, suggesting that PP_3901 is involved in the DNA damage-mediated induction of prophage genes. In this respect, the explicit regulation of PP_3901 by both LexA proteins and its involvement in the DNA damage-mediated induction of the prophage genes are reminiscent of previously described mechanisms of SOS-mediated bacteriophage induction. For instance, the Tum protein of coliphage-186 (36) and other prophages (4) has been shown to be explicitly regulated by LexA, and it controls the induction of these prophages by interfering with the lytic cycle repressor. Nonetheless, the protein sequence of PP_3901 has no apparent sequence homology with Tum, suggesting that it may be a key component of a previously unreported pathway of LexA-mediated bacteriophage induction. Moreover, induction of the prophage genes required not only the presence of PP_3901 but also treatment of the P. putida culture with mitomycin C, as shown in Fig. Fig.44 for lexA1 and lexA2 mutant derivatives. Even though both mutant derivatives had an increased amount of the PP_3901 product in nontreated cultures, the prophage gene expression remained unchanged compared with that of the isogenic wild-type strain.

FIG. 4.
Relative expression levels of PP_3873 and PP_3894 prophage genes in the P. putida wild-type (Wt) strain and PP_3901, lexA1, and lexA2 mutant derivatives of this strain measured by quantitative RT-PCR. The relative expression level is the ratio of the ...

In summary, the results presented above present a picture of pronounced asymmetry between the two cohabiting LexA regulons of P. putida and show that this asymmetry can be extended to other Pseudomonas species harboring two lexA genes. Based on previous results for the phylogeny of the mutagenesis cassette associated with the lexA2 gene (13), where the relationship between the two P. putida LexA proteins has been firmly established, the small size of the lexA2 regulon reinforces the hypothesis that the lexA2 gene resulted from a relatively ancient duplication of the full lexA-imuA-imuB-dnaE2 cassette at the onset of the β-Proteobacteria/γ-Proteobacteria radiation. As observed in other instances (5, 26), genetic duplication would have freed one of the two copies from selective constraints, while the other copy maintained its former regulatory role. This would explain both the divergence observed in the LexA2 binding motif and the very small number of genes under LexA2 regulation. Ultimately, the most convincing explanation for the survival of the lexA2 gene in several Pseudomonas and Xanthomonas species might well be its direct regulation of the imuA-imuB-dnaE2 mutagenic cassette, which has been shown to be LexA regulated in all the species in which it is present (13). In fact, in the close relative P. aeruginosa, which has lost the lexA2 gene, the imuA-imuB-dnaE2 cassette is regulated by the remaining LexA protein (9), which has been shown to correspond to P. putida LexA1 and which binds to the E. coli LexA binding sequence (9).

In this context, the fact that the P. putida LexA1 protein has an E. coli-like binding motif is noteworthy, as it confirms previous suggestions that an E. coli LexA binding motif was already in place when the lexA-imuA-imuB-dnaE2 cassette duplication took place early in the history of β- and γ-Proteobacteria (13). Furthermore, the fact that the regulon of Xanthomonas LexA1, which has a binding sequence divergent from that of E. coli (41), has been shown to regulate only a few genes (22) suggests that preservation of the E. coli LexA binding motif may have played a substantial role in the conservation of LexA regulon contents in the γ-Proteobacteria. Taking into account the significant overlap between LexA regulons in different phyla, in spite of manifestly divergent LexA binding sites across the domain Bacteria (12, 22), the evidence that motif conservation could equate to some extent with conservation of regulon contents has strong implications for the evolution of the LexA regulon, as it suggests that changes in the LexA binding sequence must have been very gradual and continuous following an ancestral line. In this context, the puzzling existence of markedly divergent LexA binding motifs (6, 7, 11, 12, 41), which are often associated with very small regulons, may be regarded simply as the end product of relaxed selection of the LexA regulon in some species and phyla.


This work was funded by grants BFM2004-02768/BMC and BFU2006-00767/BMC from the Ministerio de Educación y Ciencia de España, by grant 2005SGR533 from the Generalitat de Catalunya, and by the Consejo Superior de Investigaciones Científicas. S. Campoy is the recipient of a postdoctoral contract from INIA-IRTA. M. Abella is a recipient of a predoctoral fellowship from the Ministerio de Educación y Ciencia.


[down-pointing small open triangle]Published ahead of print on 12 October 2007.

Supplemental material for this article may be found at http://jb.asm.org/.


1. Abella, M., I. Erill, M. Jara, G. Mazon, S. Campoy, and J. Barbe. 2004. Widespread distribution of a lexA-regulated DNA damage-inducible multiple gene cassette in the Proteobacteria phylum. Mol. Microbiol. 54:212-222. [PubMed]
2. Au, N., E. Kuester-Schoeck, V. Mandava, L. E. Bothwell, S. P. Canny, K. Chachu, S. A. Colavito, S. N. Fuller, E. S. Groban, L. A. Hensley, T. C. O'Brien, A. Shah, J. T. Tierney, L. L. Tomm, T. M. O'Gara, A. I. Goranov, A. D. Grossman, and C. M. Lovett. 2005. Genetic composition of the Bacillus subtilis SOS system. J. Bacteriol. 187:7655-7666. [PMC free article] [PubMed]
3. Berg, O. G., and P. H. von Hippel. 1987. Selection of DNA binding sites by regulatory proteins. Statistical-mechanical theory and application to operators and promoters. J. Mol. Biol. 193:723-750. [PubMed]
4. Bunny, K., J. Liu, and J. Roth. 2002. Phenotypes of lexA mutations in Salmonella enterica: evidence for a lethal lexA null phenotype due to the Fels-2 prophage. J. Bacteriol. 184:6235-6249. [PMC free article] [PubMed]
5. Campoy, S., M. Fontes, S. Padmanabhan, P. Cortes, M. Llagostera, and J. Barbe. 2003. LexA-independent DNA damage-mediated induction of gene expression in Myxococcus xanthus. Mol. Microbiol. 49:769-781. [PubMed]
6. Campoy, S., G. Mazon, A. R. Fernandez de Henestrosa, M. Llagostera, P. B. Monteiro, and J. Barbe. 2002. A new regulatory DNA motif of the gamma subclass Proteobacteria: identification of the LexA protein binding site of the plant pathogen Xylella fastidiosa. Microbiology 148:3583-3597. [PubMed]
7. Campoy, S., N. Salvador, P. Cortes, I. Erill, and J. Barbe. 2005. Expression of canonical SOS genes is not under LexA repression in Bdellovibrio bacteriovorus. J. Bacteriol. 187:5367-5375. [PMC free article] [PubMed]
8. Cirz, R. T., M. B. Jones, N. A. Gingles, T. D. Minogue, B. Jarrahi, S. N. Peterson, and F. E. Romesberg. 2007. Complete and SOS-mediated response of Staphylococcus aureus to the antibiotic ciprofloxacin. J. Bacteriol. 189:531-539. [PMC free article] [PubMed]
9. Cirz, R. T., B. M. O'Neill, J. A. Hammond, S. R. Head, and F. E. Romesberg. 2006. Defining the Pseudomonas aeruginosa SOS response and its role in the global response to the antibiotic ciprofloxacin. J. Bacteriol. 188:7101-7110. [PMC free article] [PubMed]
10. Courcelle, J., A. Khodursky, B. Peter, P. O. Brown, and P. C. Hanawalt. 2001. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158:41-64. [PMC free article] [PubMed]
11. Cune, J., P. Cullen, G. Mazon, S. Campoy, B. Adler, and J. Barbe. 2005. The Leptospira interrogans lexA gene is not autoregulated. J. Bacteriol. 187:5841-5845. [PMC free article] [PubMed]
12. Erill, I., S. Campoy, and J. Barbe. 2007. Eons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol. Rev. 28:813-828. [PubMed]
13. Erill, I., S. Campoy, G. Mazon, and J. Barbe. 2006. Dispersal and regulation of an adaptive mutagenesis cassette in the bacteria domain. Nucleic Acids Res. 34:66-77. [PMC free article] [PubMed]
14. Erill, I., M. Escribano, S. Campoy, and J. Barbe. 2003. In silico analysis reveals substantial variability in the gene contents of the gamma proteobacteria LexA-regulon. Bioinformatics 19:2225-2236. [PubMed]
15. Fernandez de Henestrosa, A. R., J. Cune, G. Mazon, B. L. Dubbels, D. A. Bazylinski, and J. Barbe. 2003. Characterization of a new LexA binding motif in the marine magnetotactic bacterium strain MC-1. J. Bacteriol. 185:4471-4482. [PMC free article] [PubMed]
16. Fernandez De Henestrosa, A. R., T. Ogi, S. Aoyagi, D. Chafin, J. J. Hayes, H. Ohmori, and R. Woodgate. 2000. Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol. Microbiol. 35:1560-1572. [PubMed]
17. Galhardo, R. S., R. P. Rocha, M. V. Marques, and C. F. Menck. 2005. An SOS-regulated operon involved in damage-inducible mutagenesis in Caulobacter crescentus. Nucleic Acids Res. 33:2603-2614. [PMC free article] [PubMed]
18. Jara, M., C. Nunez, S. Campoy, A. R. Fernandez de Henestrosa, D. R. Lovley, and J. Barbe. 2003. Geobacter sulfurreducens has two autoregulated lexA genes whose products do not bind the recA promoter: differing responses of lexA and recA to DNA damage. J. Bacteriol. 185:2493-2502. [PMC free article] [PubMed]
19. Khil, P. P., and R. D. Camerini-Otero. 2002. Over 1000 genes are involved in the DNA damage response of Escherichia coli. Mol. Microbiol. 44:89-105. [PubMed]
20. Koorits, L., R. Tegova, M. Tark, K. Tarassova, A. Tover, and M. Kivisaar. 2007. Study of involvement of ImuB and DnaE2 in stationary-phase mutagenesis in Pseudomonas putida. DNA Repair 6:863-868. [PubMed]
21. Little, J. W. 1991. Mechanism of specific LexA cleavage: autodigestion and the role of RecA coprotease. Biochimie 73:411-421. [PubMed]
22. Mazon, G., I. Erill, S. Campoy, P. Cortes, E. Forano, and J. Barbe. 2004. Reconstruction of the evolutionary history of the LexA-binding sequence. Microbiology 150:3783-3795. [PubMed]
23. McNally, K. P., N. E. Freitag, and G. C. Walker. 1990. LexA-independent expression of a mutant mucAB operon. J. Bacteriol. 172:6223-6231. [PMC free article] [PubMed]
24. Miller, J. 1991. A short course in bacterial genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
25. Nelson, K. E., C. Weinel, I. T. Paulsen, R. J. Dodson, H. Hilbert, V. A. Martins dos Santos, D. E. Fouts, S. R. Gill, M. Pop, M. Holmes, L. Brinkac, M. Beanan, R. T. DeBoy, S. Daugherty, J. Kolonay, R. Madupu, W. Nelson, O. White, J. Peterson, H. Khouri, I. Hance, P. Chris Lee, E. Holtzapple, D. Scanlan, K. Tran, A. Moazzez, T. Utterback, M. Rizzo, K. Lee, D. Kosack, D. Moestl, H. Wedler, J. Lauber, D. Stjepandic, J. Hoheisel, M. Straetz, S. Heim, C. Kiewitz, J. A. Eisen, K. N. Timmis, A. Dusterhoft, B. Tummler, and C. M. Fraser. 2002. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ. Microbiol. 4:799-808. [PubMed]
26. Norioka, N., M. Y. Hsu, S. Inouye, and M. Inouye. 1995. Two recA genes in Myxococcus xanthus. J. Bacteriol. 177:4179-4182. [PMC free article] [PubMed]
27. O'Neill, M. C. 1989. Consensus methods for finding and ranking DNA binding sites. Application to Escherichia coli promoters. J. Mol. Biol. 207:301-310. [PubMed]
28. O'Neill, M. C. 1998. A general procedure for locating and analyzing protein-binding sequence motifs in nucleic acids. Proc. Natl. Acad. Sci. USA 95:10710-10715. [PMC free article] [PubMed]
29. Reppas, N. B., J. T. Wade, G. M. Church, and K. Struhl. 2006. The transition between transcriptional initiation and elongation in E. coli is highly variable and often rate limiting. Mol. Cell 24:747-757. [PubMed]
30. Ronen, M., R. Rosenberg, B. I. Shraiman, and U. Alon. 2002. Assigning numbers to the arrows: parameterizing a gene regulation network by using accurate expression kinetics. Proc. Natl. Acad. Sci. USA 99:10555-10560. [PMC free article] [PubMed]
31. Salles, B., and G. M. Weinstock. 1989. Mutation of the promoter and LexA binding sites of cea, the gene encoding colicin E1. Mol. Gen. Genet. 215:483-489. [PubMed]
32. Sambrook, J., and D. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
33. Sassanfar, M., and J. W. Roberts. 1990. Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replication. J. Mol. Biol. 212:79-96. [PubMed]
34. Sauer, R. T., M. J. Ross, and M. Ptashne. 1982. Cleavage of the lambda and P22 repressors by recA protein. J. Biol. Chem. 257:4458-4462. [PubMed]
35. Schneider, T. D., G. D. Stormo, L. Gold, and A. Ehrenfeucht. 1986. Information content of binding sites on nucleotide sequences. J. Mol. Biol. 188:415-431. [PubMed]
36. Shearwin, K. E., A. M. Brumby, and J. B. Egan. 1998. The Tum protein of coliphage 186 is an antirepressor. J. Biol. Chem. 273:5708-5715. [PubMed]
37. Smyth, G. K. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol 3:Article3. [PubMed]
38. Walker, G. C. 1984. Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol. Rev. 48:60-93. [PMC free article] [PubMed]
39. Weinel, C., K. E. Nelson, and B. Tummler. 2002. Global features of the Pseudomonas putida KT2440 genome sequence. Environ. Microbiol. 4:809-818. [PubMed]
40. Winterling, K. W., D. Chafin, J. J. Hayes, J. Sun, A. S. Levine, R. E. Yasbin, and R. Woodgate. 1998. The Bacillus subtilis DinR binding site: redefinition of the consensus sequence. J. Bacteriol. 180:2201-2211. [PMC free article] [PubMed]
41. Yang, M. K., Y. C. Yang, and C. H. Hsu. 2002. Characterization of Xanthomonas axonopodis pv. citri LexA: recognition of the LexA binding site. Mol. Genet. Genomics 268:477-487. [PubMed]
42. Yuste, L., A. B. Hervas, I. Canosa, R. Tobes, J. I. Jimenez, J. Nogales, M. M. Perez-Perez, E. Santero, E. Diaz, J. L. Ramos, V. de Lorenzo, and F. Rojo. 2006. Growth phase-dependent expression of the Pseudomonas putida KT2440 transcriptional machinery analysed with a genome-wide DNA microarray. Environ. Microbiol. 8:165-177. [PubMed]

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