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Journal of Bacteriology, November 2006, p. 7689-7695, Vol. 188, No. 21
0021-9193/06/$08.00+0     doi:10.1128/JB.00660-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Expression of the trxC Gene of Rhodobacter capsulatus: Response to Cellular Redox Status Is Mediated by the Transcriptional Regulator OxyR{triangledown}

Tanja Zeller,{dagger} Kuanyu Li,{ddagger} and Gabriele Klug*

Institut für Mikrobiologie und Molekularbiologie, University of Giessen, Heinrich-Buff-Ring 26-32, D-35392 Giessen, Germany

Received 9 May 2006/ Accepted 7 August 2006


   ABSTRACT
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Despite the importance of thioredoxins in cellular functions, little is known about the regulation of trx genes. To understand the molecular mechanisms involved in the regulation of the Rhodobacter capsulatus trxC gene, the expression of this gene was investigated. We describe OxyR-dependent redox regulation of the trxC gene that adjusts the levels of thioredoxins in the cell.


   TEXT
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Thioredoxins are small ubiquitous proteins capable of catalyzing thiol-disulfide redox reactions by a common active site sequence (Cys-Gly-Pro-Cys) (11). Together with glutaredoxins, they are responsible for maintaining a cellular reducing environment and thereby can regulate the activity of enzymes. Thioredoxins not only are involved in reducing cytoplasmic proteins but also function as singlet oxygen quenchers and hydroxyl radical scavengers (5, 14) and act as hydrogen donors for peroxidase (4). These features imply that thioredoxins have an important function in the oxidative stress response.

The thiol-reducing activities of thioredoxins have been best characterized in Escherichia coli, which harbors the trxA and trxC genes, encoding thioredoxin 1 and thioredoxin 2, respectively (16, 25). Although most of the in vivo functions of the two E. coli thioredoxins are equivalent, the transcriptional regulation of trxA and the transcriptional regulation of trxC are different (8, 21, 23, 30, 33). In E. coli, the transcriptional regulator OxyR regulates genes that respond to H2O2, including genes for thioredoxin 2 (trxC), catalase (katG), alkylhydroperoxidase (ahpCF), a small RNA (oxyS), glutaredoxin 1 (grxA), and the glutathione reductase (gorA) (36, 47). In response to the cellular redox state OxyR undergoes a dithiol/disulfide switch (37).

Previously, we showed that the two closely related species Rhodobacter sphaeroides and Rhodobacter capsulatus differ significantly in their responses to oxidative stress and in the compositions of their thioredoxin systems (17, 18). While R. capsulatus contains Trx 1 (TrxA) and Trx 2 (TrxC), R. sphaeroides lacks TrxC. Although the function of the Rhodobacter thioredoxins has been analyzed (17, 19, 27), little is known about the regulation of thioredoxin genes in phototrophic purple bacteria. The present study was undertaken to analyze the expression of the R. capsulatus trxC gene under different conditions.

Identification of regulatory regions upstream of trxC. To understand trxC regulation, it is essential to determine the corresponding promoter and cis-acting regulatory sequences. In order to localize the promoter of the trxC gene, trxC'lacZ translational fusions were constructed that contained upstream DNA sequences that were of different lengths (Table 1). ß-Galactosidase activity was measured under semiaerobic growth conditions (about 0.85 mg liter–1 dissolved oxygen) in R. capsulatus wild-type strain SB1003 as previously described (15, 24). When a trxC'lacZ fusion harboring 71 nucleotides (nt) of upstream sequence (with respect to the translational start) was expressed in trans, we observed low ß-galactosidase levels (about 8 Miller units) (Fig. 1A). Extending the length of the upstream region to 98 nt increased this activity to about 15 Miller units (Fig. 1A). Extension of the length of the upstream region to 193 and 317 nt did not further increase ß-galactosidase activities (Fig. 1A). These results suggest that there is a weak promoter for trxC expression within 71 nt 5' of the translational start and also that there are upstream sequences that influence the promoter activity. Using primer extension analysis (as described by Heck et al. [10]), a 5' end was mapped to an A at position –24 with respect to the translational start (Fig. 1B). Upstream of this A we detected DNA sequences which showed some homology to the {sigma}70 –10 and –35 promoter consensus sequence (Fig. 1B). Together, our data suggest that these sequences indeed function as a promoter for trxC transcription. However, additional regulatory DNA regions are located upstream of the trxC promoter, since ß-galactosidase activity increased when upstream regions that were 98 nt long or longer were used for trxC'lacZ fusions (Fig. 1A).


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  		TABLE 1. Bacterial strains, plasmids, and oligonucleotides used in this study

 

Figure 1
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  		FIG. 1. Analysis of trxC expression in R. capsulatus SB1003. (A) trxC expression in wild-type strain SB1003 (solid bars) and oxyR mutant SBoxyR (open bars) under semiaerobic growth conditions. ß-Galactosidase activity was determined with a series of deletions of the upstream trxC sequences fused to lacZ. The values are the means of at least 10 independent experiments. The error bars indicate standard deviations. SB71, SB1003(ptrxCup71lacZ); SB98, SB1003(ptrxCup98lacZ); SB193, SB1003(ptrxCup193lacZ); SB317, SB1003(ptrxCup317lacZ); oxyRC71, SBoxyR(ptrxCup71lacZ); oxyR98, SBoxyR(ptrxCup98lacZ); oxyR193, SBoxyR(ptrxCup193lacZ); oxyR317, SBoxyR(ptrxCup317lacZ); control SB, SB1003(pPHU236); control oxyR, SBoxyR(pPHU236). (B) Results of primer extension assays of trxC with wild-type strain SB1003 and sequence of the trxC promoter region. The arrow indicates the trxC transcriptional start site. Typical conserved –10 and –35 boxes are enclosed in boxes. –71, –98, –193, and –317 indicate the last nucleotides of the DNA fragments used for trxC'lacZ fusions.

 
trxC expression is activated by OxyR under semiaerobic and oxidative stress conditions. When the trxC'lacZ reporter constructs were transferred into the oxyR deletion strain SBoxyR (43), the ß-galactosidase activities under semiaerobic conditions were even lower than those in the wild-type strains (Fig. 1A). Whereas the ß-galactosidase activities of the wild-type strains were about 8 to 16 Miller units, the activities in SBoxyR-derived strains were approximately 6 Miller units. A plasmid that allowed expression of the oxyR gene in trans in strain SBoxyR restored wild-type levels of trxC expression [13.9 ± 0.9 Miller units for SBoxyR(ptrxCup98lacZ+oxyR), compared to 5.8 ± 0.5 Miller units for SBoxyR(ptrxCup98lacZ) and 14.7 ± 2.9 Miller units for SB1003(ptrxCup98lacZ)]. These data indicate that OxyR is involved in activation of trxC expression under semiaerobic growth conditions. Real-time reverse transcription (RT)-PCR, performed as previously described (28, 43), confirmed that trxC expression under semiaerobic conditions is indeed decreased in SBoxyR compared to wild-type strain SB1003 (about 2.5-fold decrease in trxC expression in SBoxyR).

To analyze trxC gene expression in response to oxidative stress, semiaerobically grown R. capsulatus SB1003 and SBoxyR cells were treated with 1.5 mM diamide (a thiol-specific oxidizing agent), 1.0 mM paraquat (a superoxide radical-generating compound), 1.0 mM H2O2 (a direct oxidant), and 0.6 mM tert-butyl hydroperoxide (tBOOH) (which leads to glutathione depletion [6, 32]). The survival rates under these conditions were 80 to 100% (17). Total RNA was isolated (41) at different times, and trxC expression was analyzed by real-time RT-PCR (Fig. 2A to D). In wild-type strain SB1003, >20-fold induction of trxC expression was observed after treatment with diamide for 5 min (Fig. 2A). After treatment with paraquat, the trxC level increased about sixfold within 1 min and decreased during further incubation (Fig. 2B). Treatment with H2O2 or tBOOH also led to about threefold increases in trxC expression (Fig. 2C and D). Under oxidizing conditions, higher levels of thioredoxin may be especially required since thioredoxins, together with the glutathione/glutaredoxin system, are mainly responsible for maintaining a reduced environment by reduction of disulfides (31, 37). An increase in trxC expression therefore can compensate for the glutathione depletion caused by diamide and tBOOH, as described previously for the E. coli system (3, 29). H2O2 (either directly as an added oxidant or generated by the action of the superoxide dismutase from superoxide radicals) oxidizes proteins, thereby activating the thioredoxin system. In addition, H2O2 can also be detoxified by thioredoxins (14, 35). Therefore, our data strongly suggest that under all conditions described above, induction of trxC expression is necessary to counteract oxidative stress directly and/or to compensate for depletion of the glutathione/glutaredoxin system.


Figure 2
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  		FIG. 2. (A to D) Relative expression of trxC in wild-type strain SB1003 (solid bars) and oxyR mutant SBoxyR (open bars) under oxidative stress conditions measured by semiquantitative real-time RT-PCR. The level of the trxC transcript at time zero was assigned a value of 1. Real time RT-PCR for each treatment was repeated in three independent experiments. The error bars indicate standard deviations. (E) Binding of oxidized (OxyRox) and reduced (OxyRred) OxyR protein to the trxC promoter region containing 71 nt of upstream region (trxCup71) or 98 nt of upstream region (trxCup98). To generate reducing conditions, 200 mM (final concentration) dithiothreitol was added to the reaction mixture. (Left panel) Binding of OxyR to trxCup71; (right panel) binding of OxyR to trxCup98. The following amounts of OxyR were added to the reaction mixture (total reaction volume, 20 µl): none (lane 1), 50 ng (lanes 2 and 5), 100 ng (lanes 3 and 6), and 150 ng (lanes 4 and 7).

 
In contrast to the wild-type situation, in SBoxyR trxC expression showed very little response to the different oxidative stress agents (Fig. 2A to D), suggesting that OxyR had an activating effect on trxC expression under oxidative stress conditions. OxyR has been considered to be a hydrogen peroxide-specific regulator (37), but activation of OxyR by nitrosative stress in E. coli has also been described (9). As shown in Fig. 2 A to D, our results revealed that OxyR was involved in the response to all types of oxidative agents tested, suggesting that it is not specific for a certain type of reactive oxygen species in Rhodobacter but rather reacts to changed redox conditions in the cell. Hydrogen peroxide or superoxide radicals can lead to direct oxidation of OxyR, while diamide and tBOOH lead to glutathione depletion. Since the glutathione/glutaredoxin system is involved in the reduction of OxyR (37), it is likely that diamide and tBOOH have an influence on the redox state of OxyR.

Together, our data indicate that OxyR in R. capsulatus mediates the response of trxC to oxidative stress in general, as well as the activation of trxC under normal (semiaerobic) growth conditions.

OxyR activates trxC expression by binding the trxC promoter region. It is well established that the OxyR protein affects gene expression by binding the promoter region of target genes (38, 40, 43, 47, 48). By using gel retardation assays (as described by Zeller and Klug [43]), we were able to show that purified OxyR directly binds the trxC upstream region, supporting the hypothesis that OxyR is involved in trxC gene regulation (Fig. 2E). Both oxidized and reduced OxyR bind to a DNA fragment containing at least 98 nt upstream of the trxC gene (Fig. 2E). When a DNA fragment containing only 71 nt of the upstream sequence was used, no binding was observed. Note that the same length of DNA fragments was used for both gel retardation assays and trxC'lacZ reporter genes and that slightly higher ß-galactosidase activities were observed when the 98-nt trxC upstream region was used instead of the 71-nt trxC upstream region (Fig. 1A and 2E). Therefore, our results suggest that OxyR exerts its activating effect by direct binding to the promoter of trxC in a region that is between 72 and 98 nt from the translational start. These observations also explain the very low trxC expression values when only 71 nt of the trxC upstream region was used for ß-galactosidase measurement (Fig. 1A). However, under semiaerobic conditions, only low levels of reactive oxygen species are present, and the redox state of the cell is mainly reduced. Therefore, redox-active proteins like OxyR are mainly in the reduced state (2, 45). The results of the gel retardation assays revealed that OxyR in both its oxidized and reduced forms is able to bind the trxC promoter region (Fig. 2E), indicating that reduced OxyR might alter gene expression under low-oxygen conditions. In contrast, under oxidative stress conditions, OxyR is preferentially in its oxidized form in R. capsulatus (43). Thus, in the presence of oxidative stress, trxC expression is activated mainly by oxidized OxyR. This is in agreement with the hypothesis that there is activation of gene expression by oxidized OxyR, as reported previously for several genes in various bacteria (22, 26, 37, 43, 44, 47, 48).

Deletion of trxC affects trxC expression in an OxyR-dependent manner. To see whether thioredoxin C has an effect on its own expression, we analyzed ß-galactosidase activities in the trxC mutant strain SB1003trxC after transfer of the reporter plasmids. Using 71 bp of the trxC upstream sequence, the same low ß-galactosidase activity as in the wild type was observed (Fig. 3A). However, plasmids expressing trxC'lacZ fusions with upstream regions that were at least 98 nt long exhibited 7.5- to 10-fold-increased ß-galactosidase activity in strain SB1003trxC compared to the wild type (Fig. 3A). When a plasmid allowing trxC expression in trans was transferred into strain SB1003trxC, the same trxC expression levels as in the isogenic wild type were observed [14.2 ± 5.3 Miller units for SB1003trxC(ptrxCup98lacZ+trxC), compared to 121.3 ± 23.5 Miller units for SB1003trxC(ptrxCup98lacZ) and 14.7 ± 2.9 Miller units for SB1003(ptrxCup98lacZ)]. However, this effect of trxC deletion was observed only in the presence of OxyR. Deletion of oxyR in a {Delta}trxC background (SBtrxCoxyR) did not result in the high levels of trxC expression that were observed in the trxC single mutant (Fig. 3B), indicating that the observed effect of the trxC deletion depends on the activating effect of OxyR on trxC expression (Fig. 1A).


Figure 3
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  		FIG. 3. trxC expression in wild-type strain SB1003 (solid bars) and trxC mutant SB1003trxC (gray bars) (A) and in trxC oxyR double mutant SBtrxCoxyR (open bars) and gshB mutant SB1003gshB (gray bars) (B) under semiaerobic growth conditions. ß-Galactosidase activity was determined with a series of deletions of trxC upstream sequences fused to lacZ. Since no further increase in ß-galactosidase activity was observed when the 98-nt trxC upstream region was used, we measured ß-galactosidase activity for the SBtrxCoxyR double mutant and for SB1003gshB only in the presence of the 71- and 98-nt trxC upstream regions. The values are the means of at least five independent experiments. The error bars indicate standard deviations. SB71, SB1003(ptrxCup71lacZ); SB98, SB1003(ptrxCup98lacZ); SB193, SB1003(ptrxCup193lacZ); SB317, SB1003(ptrxCup317lacZ); trxC71, SB1003trxC(ptrxCup71lacZ); trxC98, SB1003trxC(ptrxCup98lacZ); trxC193, SB1003trxC(ptrxCup193lacZ); trxC317, SB1003trxC(ptrxCup317lacZ); control SB, SB1003(pPHU236); control trxC, SB1003trxC(pPHU236); trxCoxyR71, SBtrxCoxyR(ptrxCup71lacZ); trxCoxyRC98, SBtrxCoxyR(ptrxCup98lacZ); gsh71, SB1003gshB(ptrxCup71lacZ); gsh98, SB1003gshB(ptrxCup98lacZ).

 
Such an effect of thioredoxin C could be mediated by direct binding of the protein to the promoter region of its own gene or could involve additional activating proteins/regulators, which are specifically inhibited by thioredoxin C. However, mutation of trxC could also cause changes in cellular conditions that lead to activation of trxC expression (e.g., changes in the cellular redox state).

We could not detect any significant binding of purified thioredoxin C (17) to fragments containing the 71-nt and 98-nt trxC upstream regions, using gel retardation assays. This was also true when we used reduced TrxC protein or when we used thioredoxin C together with OxyR. Since activation of trxC expression depends on OxyR (Fig. 1A and 2), we had to consider an effect of TrxC on OxyR activity. It is known that thioredoxins can regulate transcription factors such as NF-{kappa}B, AP-1 (1), or Yap1 (13) by its redox functions. Since OxyR activity depends on its redox state (37, 39, 46), direct reduction of OxyR by thioredoxin C would lead to reduced trxC expression. However, we did not observe any direct effect of thioredoxin C on the redox state of OxyR. Furthermore, coimmunoprecipitation of TrxC with OxyR failed to reveal a direct interaction between these two proteins.

The transcription of many genes is known to depend on DNA topology (7, 19, 34, 49), and it was shown previously that thioredoxin C of R. capsulatus can affect the expression of genes by inhibition of DNA gyrase activity (19). Therefore, we further analyzed whether trxC expression is dependent on gyrase activity and on DNA topology. Expression of trxC in strains SB1003trxC(ptrxCup98lacZ) and SB1003(ptrxCup98lacZ) was studied in the presence of novobiocin, a specific inhibitor of gyrase activity. Again, we did not observe a significant effect of novobiocin and therefore of DNA gyrase on the expression of the trxC gene, indicating that trxC transcription is not sensitive to DNA superhelicity and cannot explain the inhibitory effect of TrxC on its own expression. Based on the data obtained, the increased expression of trxC in a {Delta}trxC background can be explained neither by direct binding of TrxC protein to the trxC promoter region nor by a direct influence of TrxC on the redox state of OxyR or on DNA gyrase.

Influence on the cellular redox state and alterations of the OxyR redox state in the absence of TrxC. As mentioned above, thioredoxins together with the glutathione/glutaredoxin system contribute to reducing disulfide bonds in cytoplasmic proteins, thereby maintaining a reduced environment and the redox state of the cell (29, 37). In E. coli, mutations in one or both of these systems lead to changes in the cellular redox state and/or to an increase in the levels of hydrogen peroxide (2, 29). For R. capsulatus, an influence of thioredoxin C on components of the glutathione/glutaredoxin system has been reported previously (20). To confirm the hypothesis that the increase in trxC expression in SB1003trxC may be due to an altered cellular redox state, we measured ß-galactosidase activity of the trxC'lacZ fusions in SB1003gshB, a strain having a deletion in the gene encoding glutathione synthetase (20). Indeed, the ß-galactosidase activities of SB1003gshB derivatives were similar to the activities measured for SB1003trxC-derived strains (Fig. 3B). Strains of E. coli having mutations in both systems (trxA gorA and trxA gshA) were found to have constitutively active OxyR (2). If deletion of trxC alters the cellular redox state, this would also influence the redox state of OxyR and other redox-active proteins (to a more oxidized state). Since we were not able to detect native OxyR in cell extracts of R. capsulatus (because of low-affinity antibodies produced from the native R. capsulatus OxyR protein), we used an indirect approach to detect the redox state of OxyR in SB1003trxC. Previously, we showed that katG expression in R. capsulatus is activated almost exclusively by oxidized OxyR (43). In the case of an altered cellular redox state, an increase in the amount of oxidized OxyR should lead to an increase in the expression of katG. An altered redox state in strain SB1003trxC should therefore be reflected by altered katG expression even under normal, semiaerobic growth conditions. Using real-time RT-PCR, we measured the katG expression in wild-type strain SB1003 and SB1003trxC under semiaerobic conditions. Compared to the wild type, we observed a 3.9- ± 1.1-fold increase in katG expression in SB1003trxC. These results strongly suggest that deletion of trxC in R. capsulatus leads to an altered (more oxidized) redox state in the cell, thereby indirectly influencing the redox state of the transcriptional regulator OxyR. Since trxC expression is increased under oxidizing conditions (Fig. 2A to D) and oxidized OxyR is involved in this activation (Fig. 2), we concluded that the increase in trxC gene expression observed in SB1003trxC (Fig. 3) is caused by an altered OxyR redox state in SB1003trxC.

In summary, our investigations revealed that in R. capsulatus, OxyR is the main factor which determines trxC expression in response to external factors, to the level of thioredoxin C, and to the redox state of thioredoxin C, thereby adjusting thioredoxin levels in response to different stimuli.


   ACKNOWLEDGMENTS
 
This work was supported by DFG Kl563/16-1/16-2. Tanja Zeller was a recipient of a fellowship from the "Fonds der Chemischen Industrie" and the BMBF for part of the time.


   FOOTNOTES
 
* Corresponding author. Mailing address: Institut für Mikrobiologie und Molekularbiologie, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany. Phone: (49) 641 99 355 42. Fax: (49) 641 99 355 49. E-mail: Gabriele.Klug{at}mikro.bio.uni-giessen.de. Back

{triangledown} Published ahead of print on 17 August 2006. Back

{dagger} Present address: Innere Medizin III (Kardiologische Forschung), Universitätsklinikum des Saarlandes, 66421 Homburg/Saar, Germany. Back

{ddagger} Present address: Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, Bethesda, MD 20892. Back


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Journal of Bacteriology, November 2006, p. 7689-7695, Vol. 188, No. 21
0021-9193/06/$08.00+0     doi:10.1128/JB.00660-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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