Department of Microbiology & Parasitology, School of Molecular and Microbial Sciences, The University of Queensland, Brisbane, Qld 4072, Australia1
Author for correspondence: Alastair G. McEwan. Tel: +61 7 3365 4878. Fax: +61 7 3365 4620. e-mail: mcewan{at}biosci.uq.edu.au
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ABSTRACT |
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Keywords: dimethylsulfoxide respiration, gene expression, Rhodobacter capsulatus
Abbreviations: DMSO, dimethylsulfoxide; ONP, o-nitrophenol; TMAO, trimethylamine N-oxide
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INTRODUCTION |
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Recently, it has been shown that the dorCDA gene cluster is located upstream of a gene designated dorB (Shaw et al., 1999a ) and genes involved in the early steps of synthesis of the molybdenum cofactor of DMSO reductase (Solomon et al., 1999
). The dorD gene encodes a protein that is required for the biogenesis of DorA but does not have a direct role in DMSO respiration (Shaw et al., 1999a
). Upstream of dorCDA are two additional genes, dorR and dorS. Mutational analysis of the dor genes upstream of dorCDA in Rhodobacter sphaeroides (Mouncey et al., 1997
; Mouncey & Kaplan, 1998a
) has identified the sensor histidine kinase DorS and the response regulator DorR as a two-component regulatory system that is required for the DMSO-dependent induction of the dorCDA operon. A similar conclusion has been made from the analysis of a dorR mutant of R. capsulatus (Shaw et al., 1999a
). The dorR and dorC genes are divergently transcribed while the dorS gene is transcribed from a distinct promoter in the same direction as dorC (Mouncey et al., 1997
). The DorR protein is a member of the OmpR family of response regulators. In R. sphaeroides it has been shown that DorR binds to the dorRdorC intergenic region that separates these two genes in both Rhodobacter species and contains the dorCDA and dorR promoters (Ujiiye et al., 1997
; Yamamoto et al., 2001
).
A variety of environmental and nutritional signals appear to affect DMSO reductase expression. Under aerobic conditions expression of the dor operon is very low. In R. sphaeroides (Mouncey & Kaplan, 1998b ) and R. capsulatus (Shaw, 1998
) anaerobic induction appears to involve the activation of dorS expression by the transcriptional regulator FNR. An FNR-binding site has been identified upstream of dorS in R. sphaeroides (Mouncey & Kaplan, 1998b
) while no such binding site has been found in the dorRdorCDA intergenic region of either Rhodobacter species. In addition, Mouncey & Kaplan (1998a
) have shown that negative aerobic regulation of dor expression in R. sphaeroides is under redox control via the cytochrome cbb3 oxidase, although the details of this signal transduction pathway are not entirely clear. Recently, we showed that the ModE orthologue in R. capsulatus, MopB, was also required for high levels of dor operon expression in this organism (Solomon et al., 2000
). MopB activates dor expression in the presence of molybdate and is also required for molybdate-dependent repression of the alternative nitrogenase (Wang et al., 1993
). Clearly, regulation of the dor anaerobic respiratory system is complex, and appears to be linked to other major bioenergetic and metabolic processes in phototrophic bacteria.
In this study we have investigated in more detail the regulation of DMSO reductase expression via the response regulator DorR. An emerging phenomenon over the last few years has been the control of the phosphorylation state of response regulators by small metabolites such as acetyl phosphate (McCleary & Stock, 1994 ; Prüß, 1998
). This metabolic control of response regulators provides an additional element in the signal transduction pathways of some sensor kinaseresponse regulator systems. In view of the key role of DMSO respiration in anaerobic dark growth of R. capsulatus we here consider the possibility that DorR may be under this form of metabolic control. A second aim was to determine whether the negative control of dor operon expression was dependent upon the global, redox-responsive RegBA histidine kinaseresponse regulator system (Swem et al., 2001
; Elsen et al., 2000
). Here we report that the regulation of dor operon expression is dependent upon the DorR protein, and is integrated into the RegBACco redox-regulatory system.
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METHODS |
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Molecular biological methods.
Plasmids pSL111 and pALS69, harbouring dorA::lacZ and dorR::lacZ transcriptional fusions, respectively, have been described by Shaw et al. (1999a ) and Shaw (1998)
. Plasmids were transferred into R. capsulatus by biparental matings (Simon et al., 1983
) using E. coli S17-1 as donor strain.
DMSO reductase activity
This was measured in extracts of total soluble protein, using dithionite-reduced methylviologen as electron donor (McEwan et al., 1985 ). One unit of activity corresponds to 1 µmol methylviologen oxidized min-1. All measurements were carried out at least in triplicate on each cell extract and are the means of three independent growths (four in the case of the reg mutant strain).
ß-Galactosidase activity.
In time-course growth experiments and aerobic/anaerobic shift experiments the activity of chromosomal lacZ fusions was determined by the method of Miller (1972) , using chloroform and cetyltrimethylammonium bromide (CTAB). In all other experiments, ß-galactosidase activity was determined as nmol ONP (mg protein)-1, using the method of Clark & Switzer (1977)
. All measurements were carried out in triplicate on each cell extract and are the mean of at least two independent growth experiments. Protein was determined by the Lowry method or using the bicinchoninic acid assay (Sigma). Denaturing polyacrylamide gel electrophoresis and Western blotting were performed using standard procedures (Sambrook et al., 1989
). Anti-DMSO reductase antibodies were used as described by Hatton et al. (1994)
.
Growth experiments.
Measurements of bacterial growth were carried out under high-light (100 W m-2) and low-light (16 W m-2) conditions at 30 °C as described by Horne et al. (1996) for the dorR mutant, the regA mutant strain and their respective wild-type strains with either malate or pyruvate as carbon source. Experimental cultures were prepared by inoculating 100 ml medium with 2% (high light) or 5% (low light) of a pre-culture grown up under the conditions to be used for the main experiment and incubated as described above. Samples (1 ml) for optical density measurements (with a Hitachi U-3000 spectrophotometer) were removed at intervals suitable to the respective growth rate (between 1 h and 4 h). Cultures were topped up with the respective growth medium after sampling. All experiments were repeated at least twice. For experiments involving a shift from dark aerobic to dark anaerobic growth, 100 ml medium was shaken in 1 l flasks (30 °C, 200 r.p.m.) until an OD680 of 0·30·5 was reached. Cultures were then transferred to sterile 100 ml bottles and incubated at 30 °C in the dark.
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RESULTS |
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Pyruvate activates dor operon expression via DorR at low light intensity and under aerobic conditions
Since DMSO respiration is a key activity associated with anaerobic dark growth using fermentable carbon sources in R. capsulatus we determined whether a carbon source that produced phosphorylated intermediates such as acetyl phosphate might exert an effect on dor operon expression. Fig. 2 shows that DMSO reductase activity in DMSO-induced R. capsulatus 37b4 cells grown at high light intensity was reduced by 50% when pyruvate replaced malate as carbon source. Time-course induction experiments confirmed that this result was not dependent on the growth phase of the culture (data not shown). Under low-light conditions DMSO reductase activity in DMSO-induced wild-type cells was similar in cells grown on either carbon source. However, in the absence of DMSO, the activity level in wild-type cells grown at low light intensity was about 10-fold higher in cells grown on pyruvate and was similar to the level found in the dorR mutant grown on malate. In this mutant the DMSO reductase activity levels observed were comparable to those found in cells grown on malate, and there also appeared to be a slight effect of light intensity on enzyme expression. It is worth noting that the aerobic repression of the dor operon also seemed to be less stringent with pyruvate as carbon source (Fig. 2
).
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DMSO reductase expression is repressed by the response regulator RegA
The RegBA system is a global regulator of gene expression in Rhodobacter species. It has a key role in the induction of the photosynthetic apparatus (Sganga & Bauer, 1992 ; Du et al., 1998
) and has also been shown to modulate expression of nitrogen and carbon dioxide fixation pathways, the uptake hydrogenase and proteins involved in respiratory processes (Elsen et al., 2000
; Qian & Tabita, 1996
; Swem et al., 2001
). Recently it has also been demonstrated that wild-type RegA controls activity of the puf and puc promoters directly by binding to the relevant sequences (Hemschemeier et al., 2000
). It had been previously observed that DMSO reductase activity in R. sphaeroides is influenced by mutations in the rdx and cco operons (Mouncey & Kaplan, 1998a
), and a direct interaction between components of these operons and the sensor kinase DorS had been suggested by the authors. As recent studies have established an involvement of the RegBA regulatory system (known as PrrBA in R. sphaeroides) in the transmission of signals generated by components of the cco and rdx operons (OGara & Kaplan, 1997
; Roh & Kaplan, 2000
), the effect of a mutation in the regA gene on DMSO reductase expression was investigated. Measurements of DMSO reductase activity of R. capsulatus wild-type (strain SB1003) and regA mutant strain MSO1 (Sganga & Bauer, 1992
), grown under phototrophic (high light) conditions in the absence of DMSO showed that activity was increased in the regA mutant, reaching levels comparable to that found in DMSO-induced wild-type cells (Fig. 3a
). In DMSO-induced cultures a further twofold increase of activity was observed in the mutant (Fig. 3a
). The presence of DMSO reductase in the regA mutant strain grown in the absence of DMSO was confirmed by Western blotting (Fig. 3a
). In a corresponding set of experiments the activity of a dorA::lacZ gene fusion in the regA mutant background was determined and was also found to be higher than that of a wild-type genetic background (Fig. 4a
). This result confirmed that regA was exerting an effect on the transcription of the dor operon. These data suggest that the RegBA system is involved in repression of dor operon expression and that RegA might be acting as a repressor.
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The cytochrome cbb3 oxidase is a negative regulator of dor operon expression
Having shown that a mutation in the regA resulted in deregulation of dor expression, we investigated whether the observed effect is part of a redox-signalling pathway involving cytochrome cbb3. It is already established that the cytochrome cbb3 oxidase is a key regulator of anaerobic gene expression in R. sphaeroides (Oh & Kaplan, 1999 ; Mouncey & Kaplan, 1998a
; Oh & Kapla
n, 2001
). In R. capsulatus, dor operon expression, as indicated by the level of
[dorA::lacZ] activity, was about twofold higher in a cco mutant compared to the wild-type strain. However, the most obvious difference between the two strains was the sixfold amplification in
[dorA::lacZ] activity that was observed upon addition of DMSO. This was only observed in the cco mutant at high light intensity. At low light intensity
[dorA::lacZ] activity was much higher in both strains even under non-induced conditions, and no difference between induced and non-induced activity levels was observed for the cco mutant.
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DISCUSSION |
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The low level of expression of DMSO reductase under aerobic conditions in both the wild-type and the dorR mutant strain may be partly due to the failure to express the DorS sensor, since the dorS gene is under FNR control (Mouncey & Kaplan, 1998a ). This would prevent a high level of phosphorylated DorR from being generated. Support for the suggestion that it is a limitation in the phosphorylated form of DorR that limits dor operon expression comes from the observation that in the presence of pyruvate elevated levels of DMSO reductase can be measured under aerobic conditions. The simplest explanation for this result is the phosphorylation of DorR by acetyl phosphate produced from pyruvate metabolism. Such a situation would allow the DorR protein to act as a positive regulator in the absence of the sensor DorS. It is established in E. coli that acetyl phosphate levels can vary greatly in cells, depending on carbon source, and under some circumstances can be as high as 1 mM (McCleary & Stock, 1994
). Acetyl phosphate has also been shown to be involved in the regulation of OmpR-mediated processes in E. coli (Prüß, 1998
). A similar mechanism might be involved in the effects observed with respect to DorR in our experiments.
Two modes of anaerobic dark growth have been described for R. capsulatus, namely anaerobic respiration using DMSO or TMAO, and fermentative growth in the presence of bicarbonate. Of these two modes, anaerobic respiration is the more energetically favourable one, allowing growth to higher cell densities. A twofold induction of dorR and dorA expression was observed when aerobically grown cells were shifted to anaerobic conditions, suggesting that the dor respiratory system might be involved in regulation of this growth mode. However, subsequent experiments using a dorR mutant showed clearly that the two dark anaerobic growth modes are unrelated, and DorR is not involved in general regulation of dark anaerobic growth. The observed increase in expression might be caused by a relaxation of the aerobic repression of dor operon expression.
DMSO respiration is a key energy generator under anaerobic dark conditions but the superiority of photophosphorylation and oxidative phosphorylation with oxygen as electron acceptor has led to the evolution of mechanisms that ensure that dor operon expression is negatively controlled by light and oxygen. A major factor in this control is the cytochrome cbb3 oxidase since a cco mutant exhibits higher levels of dor operon expression under both aerobic and phototrophic conditions. A similar result has been reported by Mouncey & Kaplan (1998a ), and this group has recently suggested that redox signals are transduced via the CcoQ protein to the PrrBA two-component system (the homologue of the RegBA system in R. capsulatus). The pathway transducing the signal generated by the cytochrome cbb3 oxidase has also been shown to influence the expression of photosynthesis and accessory pigments (Oh & Kaplan, 1999
; OGara et al., 1998
). Investigation of dor operon expression in a regA mutant showed a very significant deregulation of DMSO reductase expression, with the non-induced mutant strains reaching activity levels comparable to those found in induced wild-type cells. The pattern of DMSO-dependent induction of expression, however, remained the same. Together these results indicate that DMSO reductase expression is negatively regulated by a signal generated by the cytochrome cbb3 oxidase, and that this signal is transmitted via the RegBA two-component system rather than by direct interaction of CcoQ with the DorS sensor kinase, as had been suggested for R. sphaeroides (Mouncey & Kaplan 1998a
). The way in which RegA influences dor operon expression remains to be determined; examination of the dorRdorC intergenic region for a RegA binding consensus sequence, recently described by two groups (Emmerich et al., 2000
; Swem et al., 2001
), failed to identify any such site.
An interesting finding with regard to dor operon regulation is that the deregulation of DMSO reductase observed in the malate-grown regA mutant strain can be reversed by a change of carbon source; when this strain was grown with pyruvate as carbon source, the familiar regulation pattern for DMSO reduction was restored. In the regA mutant, expression levels in the absence of DMSO were very low, while addition of DMSO led to a strong induction of activity. Both malate and pyruvate are substrates that are slightly more oxidized than the cell carbon, and the main difference in their utilization pathways is that pyruvate gives rise to enhanced levels of acetyl phosphate. Acetyl phosphate has been shown to be involved in metabolic control in enteric bacteria (Bouché et al., 1998 ; Nyström, 1994
; Prüß, 1998
), and is known to act as a phosphate donor to some response regulators. However, it is unlikely that the effect observed in the pyruvate-grown regA mutant is due to an increase in phosphorylated DorR, as that should result in increased DMSO reductase expression rather than a re-establishment of control mechanisms. We therefore suggest that another regulatory circuit is activated by acetyl phosphate and causes the observed repression of DMSO reductase expression.
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ACKNOWLEDGEMENTS |
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Received 24 September 2001;
accepted 18 October 2001.