Department of Bacteriology, University of WisconsinMadison, Room 390B, 420 Henry Mall, Madison, WI 53706, USA
Correspondence
Timothy J. Donohue
tdonohue{at}bact.wisc.edu
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ABSTRACT |
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INTRODUCTION |
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R. sphaeroides is an alphaproteobacterium that grows by respiration in the presence or absence of O2 or by photosynthesis when light is present under anaerobic conditions (Zeilstra-Ryalls et al., 1998). In this or related photosynthetic bacteria, PrrA target genes encode components of the photosynthetic apparatus (Eraso & Kaplan, 1994
), cytochrome oxidases that conserve energy at low O2 tensions (Eraso & Kaplan, 2000
), electron carriers like cytochrome c2 that function in respiration and photosynthesis (Comolli et al., 2002
; Karls et al., 1999
; Swem et al., 2001
) and proteins that use reducing power under anoxic conditions (Dubbs et al., 2000
; Joshi & Tabita, 1996
; Qian & Tabita, 1996
).
Homologues of PrrA exist in alpha- and gammaproteobacteria, where they act in homeostatic control circuits to regulate gene expression in response to changes in the oxidationreduction state of the aerobic electron transport chain (Bauer et al., 1998; Comolli et al., 2002
; Comolli & Donohue, 2002
; Elsen et al., 2004
). PrrA is phosphorylated by the membrane-bound histidine kinase PrrB (Bird et al., 1999
; Comolli et al., 2002
; Eraso & Kaplan, 1995
, 1996
; Oh et al., 2004
; Potter et al., 2002
). A terminal oxidase within the aerobic respiratory chain, the cytochrome cbb3 oxidase, is able to control the phosphatase activity of PrrB (Oh et al., 2004
), increasing the amount of phosphorylated PrrA when O2 is limiting (Oh & Kaplan, 2000
, 2001
; Oh et al., 2004
).
Response regulators functioning as transcription factors often contain a C-terminal DNA-binding domain related to Escherichia coli OmpR or NarL (Hakenback & Stock, 1996; Kenney, 2002
; Stock et al., 2000
). However, the PrrA C-terminal domain (PrrA-CTD) does not contain significant amino acid sequence similarity to the DNA-binding domains of well-studied response regulators (Elsen et al., 2004
; Eraso & Kaplan, 1994
). Computational analysis of the PrrA-CTD suggests that there is amino acid sequence similarity to the DNA-binding domain of E. coli Fis (Fig. 1
). Indeed, NMR analysis of the PrrA-CTD revealed that it forms a three-helix bundle with a helixturnhelix DNA-binding domain (Laguri et al., 2003
). In addition, the helixturnhelix of the PrrA-CTD showed the greatest degree of structural similarity to Fis when compared to other transcription factors for which structures are available (Laguri et al., 2003
).
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METHODS |
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PrrA purification.
PrrA proteins were expressed as intein fusions in ER2566 (Comolli et al., 2002). An 800 ml culture was grown (37 °C) until an OD600 of 0·50·8, 0·3 mM IPTG was added and the culture was then shaken at 30 °C for 3 h. Cells were harvested by centrifugation, resuspended in 15 ml column buffer (20 mM Tris/HCl, pH 8·0, 0·1 mM EDTA, 0·5 M KCl, 0·1 % Triton X-100, 5 mM MgCl2) and lysed by sonication. The extract was centrifuged for 30 min at 13 000 g (4 °C) and the supernatant was loaded onto a 10 ml chitin column previously equilibrated with 10 vols column buffer. The column was washed with 10 vols column buffer before overnight treatment (4 °C) with 35 ml column buffer supplemented with 0·3 mM DTT to stimulate cleavage of the intein domain. The column was washed with column buffer and 4 ml fractions were collected. An aliquot of each fraction was analysed on 12 % Bis-Tris SDS gels (Invitrogen). PrrA-containing fractions were pooled, dialysed into PrrA buffer (40 mM Tris/HCl, pH 7·9, 5 mM MgCl2, 50 mM KCl, 0·1 mM DTT) and then into PrrA buffer containing 25 % glycerol for storage at 80 °C. Protein concentrations were determined by the Bradford assay using BSA as a standard (Bio-Rad).
PrrA phosphorylation.
PrrA proteins (15 µM final concentration) were added to transcription buffer (10 mM Tris/HCl, pH 8·0, 10 mM MgCl2, 1 mM EDTA, 0·3 mM DTT), supplemented with 0·1 mg BSA ml1 and 0·1 mM DTT in a final volume of 25 µl. 32P-labelled acetyl phosphate was added to 25 mM and the mixture was incubated at 30 °C for 45 min (McCleary & Stock, 1994). To assay PrrA phosphorylation, 10 µl 3x SDS stop solution (Comolli & Donohue, 2002
) was added, the samples were analysed on 12 % Bis-Tris SDS gels (Invitrogen) and radioactivity in PrrA was measured by phosphorimaging (Molecular Dynamics).
In vitro transcription.
R. sphaeroides RNA polymerase holoenyzme was prepared by heparin agarose chromatography (Anthony et al., 2003). Multiple-round in vitro transcription assays used
70 nM RNA polymerase, acetyl phosphate-treated PrrA, 20 nM cycA P2 template plasmid (pRKK146) or puc template plasmid (pJC412) in a 20 µl reaction containing transcription buffer, 0·1 mM DTT and 0·1 mg BSA ml1. These components were incubated for 20 min at 30 °C and the reaction was initiated by adding nucleoside triphosphates (0·5 mM ATP, 0·5 mM CTP, 0·5 mM GTP and 50 µM UTP) plus 10 µCi [
-32P]UTP. After incubation for 20 min at 30 °C, the reaction was terminated by adding 10 µl gel-loading buffer (95 % formamide, 20 mM EDTA, 0·05 % bromophenol blue and 0·05 % xylene cyanol). The samples were placed at 95 °C for 3 min and analysed on a 6 % polyacrylamide, 7 M urea gel alongside DNA sequencing reactions to map the transcription start site for individual promoters. Transcript abundance was quantified by phosphorimaging. PrrA proteins were phosphorylated by mixing 25 µM PrrA with 25 mM acetyl phosphate in transcription buffer for 60 min at 30 °C.
DNase I footprinting.
A 32P-labelled cycA P2 DNA fragment (extending from 228 to +22 relative to the known transcription initiation site; Karls et al., 1999; Newlands et al., 1991
) was obtained by digesting pRKK128 with HindIII and NotI followed by labelling the HindIII restriction site with [
-32P]dATP. The DNA fragment was gel-purified and then treated with DNase I (approx. 510 nM) for 30 s in transcription buffer in the absence or presence of acetyl phosphate-treated PrrA (Karls et al., 1999
; Newlands et al., 1991
). Prior to electrophoresis, 10 µl gel-loading buffer was added to the samples and they were heated at 95 °C for 45 s. Samples were analysed on a 6 % polyacrylamide, 7 M urea gel alongside DNA sequencing reactions to localize the relative position of PrrA-binding sites. Radioactivity was visualized and quantified by phosphorimaging.
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RESULTS |
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To analyse the mutant PrrA proteins, each was expressed as an intein fusion and purified by a protocol used previously for purification of wild-type PrrA (Comolli et al., 2002). The yield and purity (>95 % pure by SDS-PAGE) of most of the mutant proteins was comparable to wild-type PrrA (data not shown). However, PrrA-N168G and PrrA-L174A were obtained at
2-fold lower yields (
20 µM final concentration) relative to wild-type PrrA or the other mutant PrrA proteins.
Acetyl phosphate-treated wild-type or mutant PrrA proteins, when analysed by molecular sieve chromatography (Superdex 200; 25 mM Tris/HCl, pH 7·9, 150 mM NaCl), eluted at the apparent molecular mass expected for a PrrA monomer (data not shown). Thus, there is no evidence that any of these amino acid substitutions caused significant aggregation or alterations in the apparent oligomeric state of the protein (data not shown).
Many response regulators acting as transcription factors require phosphorylation to activate transcription (Kenney, 2002; Stock et al., 2000
). If any amino acid substitutions in the PrrA-CTD caused dramatic changes in the overall conformation of the protein, they might alter the capacity of the protein to be phosphorylated. To test for such changes, we monitored the ability of the mutant PrrA proteins to accept phosphate from 32P-acetyl phosphate, a low-molecular-mass phosphate donor. Wild-type PrrA is phosphorylated by acetyl phosphate in vitro and the phosphorylated protein is sufficiently stable (t0·5
330 min) to monitor this modification by SDS-PAGE (Comolli et al., 2002
). Under our assay conditions, most of the mutant PrrA proteins were labelled to
50 % of the level observed for wild-type PrrA (Table 2
). The only exceptions were PrrA-H170A and PrrA-L174A, which were labelled at a level
3-fold lower than wild-type PrrA (Table 2
).
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We also assayed the ability of PrrA proteins to stimulate transcription from the puc promoter (Eraso & Kaplan, 1994), which is directly activated by RegA, a PrrA homologue from Rhodobacter capsulatus (Bowman et al., 1999
). Unlike cycA, there was detectable puc-specific transcript produced in the absence of acetyl phosphate-treated wild-type PrrA (Fig. 3
). Transcript abundance increased in the presence of acetyl phosphate-treated wild-type PrrA, with maximal levels at
2·5 µM protein when compared to the control RNA1 product (Fig. 3
).
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DNA binding by mutant PrrA proteins
To test whether any of these amino acid substitutions altered DNA binding, we assayed the ability of acetyl phosphate-treated PrrA proteins to bind cycA P2 by DNase I footprinting. Previous experiments demonstrated that a mutant form of the R. capsulatus PrrA homologue, RegA*, which has increased activity in the absence of phosphorylation (Du et al., 1998; Karls et al., 1999
), protected a single region of cycA P2 from DNase I digestion (Karls et al., 1999
). Analysis of wild-type PrrA binding to cycA P2 showed that
12 µM acetyl phosphate-treated protein was sufficient to protect a
20 bp region on the top strand that is centred at 51 (Fig. 4
). The region of cycA P2 protected from DNase I digestion matches the region protected by RegA* previously (Karls et al., 1999
).
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Acetyl phosphate-treated PrrA-N168A and PrrA-I177A proteins each protected the same 20 bp region from DNase I digestion as seen when using acetyl phosphate-treated wild-type PrrA protein (Fig. 4
). In addition, DNase I protection of cycA P2 by PrrA-N168A protein was detectable at
1 µM, whereas protection by PrrA-I177A was detectable at
2 µM. When comparing the change in intensity of DNase I cleavage products in a region of the promoter that was not protected by acetyl phosphate-treated PrrA (92 to 72) to that protected by acetyl phosphate-treated protein (61 to 45), it appeared that PrrA-N168A, PrrA-I177A and wild-type PrrA each saturated cycA P2 at concentrations between
2 and 4 µM (Fig. 4
). The similar apparent affinity of PrrA-N168A for cycA P2 is not surprising, since it has essentially wild-type activity for activation of this promoter. However, a similar apparent affinity of PrrA-I177A and wild-type PrrA for cycA P2 is surprising, since this mutant protein was defective in activating this promoter in vitro (see above).
The other acetyl phosphate-treated mutant PrrA proteins tested (PrrA-R171A, PrrA-T173A, PrrA-L174A and PrrA-L178A) were unable to protect the cycA P2 promoter from DNase I digestion even when using 4-fold more acetyl phosphate-treated protein than was needed to occupy this site with wild-type PrrA. The inability to detect significant binding of PrrA-R171A, PrrA-T173A, PrrA-L174A or PrrA-L178A to this promoter is consistent with their inability to activate cycA P2 transcription at any of the concentrations tested (see above).
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DISCUSSION |
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Amino acids in the turn of the PrrA C-terminal helixturnhelix motif
PrrA N168, M169 and H170 form the turn between helices 1 and 2 (Laguri et al., 2003). We found the side chains at residues 169 and 170 to be important for PrrA function, since PrrA-M169A and PrrA-H170A each exhibited significant defects in activating transcription at the two target promoters tested. In contrast, PrrA-N168A produced transcripts from both PrrA-dependent promoters at levels comparable to that produced by similar concentrations of the wild-type protein. However, even at high concentrations, PrrA-N168G only partially activated both of the PrrA-dependent promoters. The diminished activity of PrrA-N168G is surprising, since glycine is often found in the first position of the turn between helices 1 and 2 of helixturnhelix DNA-binding proteins (Brennan & Matthews, 1989
). While many PrrA homologues contain an asparagine at the position analogous to PrrA N168, some, including Pseudomonas aeruginosa RoxR (Fig. 1
), contain a glycine at the analogous position (Comolli et al., 2002
; Comolli & Donohue, 2002
; Elsen et al., 2004
). Indeed, amino acid sequence alignments propose that family members containing a glycine at the position equivalent to PrrA N168 are in a second group of PrrA homologues (Comolli et al., 2002
; Comolli & Donohue, 2002
; Elsen et al., 2004
). The group 2 PrrA homologue P. aeruginosa RoxR substitutes for R. sphaeroides PrrA in vivo and in vitro (Comolli et al., 2002
; Comolli & Donohue, 2002
; Elsen et al., 2004
), so the amino acid side chain at this position is not absolutely required for function in either organism. However, there may be other, unknown features of PrrA homologues that allow the protein to function with either a glycine or asparagine at the first position in the turn before helix 2. For example, side-chain differences at other positions between group 1 and group 2 PrrA homologues may allow proper helix 1helix 2 positioning in other members of this family. In this regard, the residue analogous to PrrA Y153, which makes side-chain interactions with both L178 and L174 (see below), is a leucine in P. aeruginosa RoxR (Fig. 1
).
The effects of alanine substitutions in residues that stabilize helixhelix interactions in the PrrA-CTD
The structure of the PrrA-CTD predicts that the L174 and L178 side chains (helix 2) make hydrophobic interactions with side chains of residues T163 and Y153 (helix 1), respectively (Laguri et al., 2003). Both PrrA-L174A and PrrA-L178A failed to activate cycA P2 transcription detectably and to protect cycA P2 from digestion by DNase I. Because of this, we propose that the loss of a single leucine side chain is sufficient to decrease high-affinity DNA binding at cycA P2, presumably by destabilizing helix 1helix 2 interactions.
We also found that PrrA-I177A only partially activated transcription of both promoters tested, even though this protein protected cycA P2 from DNase I digestion at concentrations identical to wild-type PrrA. The I177 side chain is predicted to make hydrophobic contacts with W146, a residue within the three-helix bundle of the PrrA-CTD (Laguri et al., 2003). PrrA I177 is also located near the C terminus of the DNA-binding helix, so the PrrA-I177A substitution could cause a partial activation defect by altering a proteinprotein interaction, either within the PrrA-CTD itself, with DNA or by altering some other step in transcription.
The effects of alanine substitutions in the potential DNA-binding residues of the PrrA-CTD
Models of PrrAtarget site interactions predict that surface-exposed side chains of residues R171, R172, Q175 and R176 make sequence-specific contacts with DNA (Laguri et al., 2003; Pan et al., 1994
, 1996
). In the case of Fis, the analogous side chains of residues R85, K89 and K90 are mapped in close proximity to DNA based on copper(I) ortho-phenanthroline cleavage (Pan et al., 1994
, 1996
). PrrA proteins with alanine substitutions in R171, R172, Q175 or R176 exhibited little or no detectable activation of cycA P2 or puc transcription. In addition, PrrA-R171A could not protect cycA P2 from DNase I protection at any concentration tested. Thus, the properties of PrrA-R171A, PrrA-R172A, PrrA-Q175A and PrrA-R176A support the notion that these residues constitute part of the DNA-recognition helix (Laguri et al., 2003
).
It is not known how residues T173 and K180 contribute to PrrA function, but the analogous residues in Fis (T87 and K94) are proposed to interact with the DNA phosphate backbone (Pan et al., 1994, 1996
; Yuan et al., 1991
). Based on the structural similarity between the PrrA-CTD and Fis, we propose that the inability of PrrA-K180A to activate transcription reflects the loss of a positively charged side chain required to make phosphate backbone contacts. We also propose that the T173 side chain makes polar contacts with DNA, since PrrA-T173A only partially activated transcription and did not protect cycA P2 from DNase I digestion at the concentrations tested.
In summary, our findings support the recent proposal for function of the helixturnhelix motif in the PrrA-CTD in DNA binding (Laguri et al., 2003). However, the behaviour of individual mutant PrrA proteins suggests that features in the turn preceding helix 2 are different within other members of this family or atypical compared with other helixturnhelix transcription factors. Our data also pose additional questions about the interaction of amino acid side chains within helix 2 of the PrrA-CTD and either target DNA or RNA polymerase. The ability to analyse the structure and function of mutant PrrA proteins makes it possible to obtain molecular insights into how this global regulator of energy-conserving pathways binds DNA and activates transcription. The presence of PrrA homologues in many facultative bacteria (Comolli et al., 2002
; Comolli & Donohue, 2002
; Elsen et al., 2004
) means that this information can provide new insights into how free-living bacteria or those that interact with plant or animal cells control expression of energy-conserving pathways.
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ACKNOWLEDGEMENTS |
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Received 24 June 2005;
revised 16 August 2005;
accepted 5 September 2005.
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