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Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada R3T 2N2
Correspondence
Elizabeth A. Worobec
eworobe{at}ms.umanitoba.ca
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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-galactosidase reporter gene fusions in response to 5, 8 and 10 % sucrose, 1, 5 and 8 mM salicylate, and different pH and temperature values. -Galactosidase activity assays revealed that a lower growth temperature (28 °C), a more basic pH (pH 8), and an absence of sucrose and salicylate induce the transcription of the ompF gene, whereas the induction of ompC is stimulated at a higher growth temperature (42 °C), acidic pH (pH 6), and maximum concentrations of sucrose (10 %) and salicylate (8 mM). In addition, when multiple conditions were tested, temperature had the predominant effect, followed by pH. In this study, it was found that the MicF regulatory mechanism does not play a role in the osmoregulation of the ompF and ompC genes, whereas MicF does repress OmpF expression in the presence of salicylate and high growth temperature, and under low pH conditions.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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-Lactam resistance in this organism is due in part to -lactamase enzymes (Sanders & Sanders, 1992
); however, a reduction in the levels of outer membrane porins is also responsible for altering resistance levels by decreasing the outer membrane permeability (Gutmann et al., 1984).
Our group has characterized two S. marcescens porins, OmpC and OmpF (Hutsul & Worobec, 1997), with molecular masses of 40 and 41 kDa, respectively. These porins are non-specific protein channels that serve to take in nutrients and antibiotics, such as -lactams, and export waste products. OmpF is believed to have a slightly larger pore diameter, resulting in a faster rate of diffusion through OmpF than through OmpC. The structural genes for both OmpF and OmpC have been cloned and sequenced. S. marcescens OmpC and OmpF are 71 % and 68 % similar to Escherichia coli OmpC and OmpF, respectively, at the amino acid level (Hutsul & Worobec, 1997).
The production of E. coli OmpF and OmpC is regulated by many environmental factors, such as osmotic pressure, temperature and pH. Production of the appropriate outer membrane porin is required for survival of the organism under widely differing conditions (Csonka, 1989). For example, in the human gut, where concentrations of both nutrients and toxic products, such as bile salts, are relatively high, OmpC is the predominant porin. In a nutrient-poor environment, such as fresh water, OmpF is the major porin species (Mizuno & Mizushima, 1990; Pratt & Silhavy, 1995). High osmotic pressure, high temperature, low pH and higher concentrations of salicylate favour the expression of E. coli OmpC over OmpF (Pratt et al., 1996).
The most extensively studied mechanism of porin regulation in E. coli is a two-component regulatory system composed of an inner membrane sensor protein called EnvZ, and a response regulator, OmpR (Batchelor et al., 2004; Cai & Inouye, 2002; Pratt & Silhavy, 1995; Mizuno & Mizushima, 1990). EnvZ monitors the external osmolarity, and communicates this information to OmpR by phosphorylation and dephosphorylation. In its phosphorylated state, OmpR-P regulates transcription from the ompF and ompC genes. Under conditions of high osmolarity, OmpR-P represses transcription of ompF, and activates ompC transcription, while under conditions of low osmolarity, OmpR-P activates transcription of ompF (Aiba et al., 1989). The difference in transcriptional activation is a result of the differential organization of the OmpR-binding sites (OBSs) upstream of the two porin genes, with ompF having an additional OBS (Harlocker et al., 1995). The OBSs also have different affinities, such that at low levels of OmpR-P, the higher-affinity sites of ompF are preferentially bound by OmpR, and transcription is activated, while at higher levels of OmpR-P, the lower-affinity sites of ompC are bound, resulting in increased transcription (Liu & Ferenci, 2001; Harlocker et al., 1995). In addition, when the low-affinity upstream site of ompF is bound by OmpR-P, the integration host factor (IHF) helps to form a DNA loop that stalls the transcription of the ompF gene (Ramani et al., 1992). As a result, as external osmolarity increases, the levels of OmpC increase, while those of OmpF decrease.
In E. coli, OmpF levels also decrease with increased growth temperature (Andersen et al., 1989), and in the presence of salicylate (Nikaido, 2003; Rosner et al., 1991). These conditions involve the antisense RNA, micF (mRNA interfering complementary RNA). The micF gene is located immediately upstream of ompC, and is transcribed in the opposite direction (Mizuno et al., 1984). Two species of RNA exist due to two promoters upstream of micF, which result in a 93 nt 4·5S RNA, and a 174 nt 6S RNA. The 4·5S RNA product of the micF gene forms a stable duplex with the RBS of ompF mRNA, thus inhibiting ompF translation, and destabilizing the mRNA (Schmidt et al., 1995; Andersen & Delihas, 1990). Transcription of micF is activated by OmpR at the same regulatory sites as those involved in ompC transcription (Coyer et al., 1990). In E. coli, micF transcription has been shown to decrease under conditions of low osmolarity (Takayanagi et al., 1991), lower temperature (Forst & Inouye, 1988; Delihas & Forst, 2001), and decreased weak acid concentrations (Pratt et al., 1996).
Based on the inherent similarities between S. marcescens and E. coli OmpF and OmpC porins, we decided to investigate the expression of S. marcescens ompF and ompC genes in the presence of different environmental factors, including osmotic pressure, temperature, pH and salicylate. In addition, we addressed the possibility that the MicF regulatory system might play a role in controlling the expression of S. marcescens ompC and ompF genes.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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. pOYL338W, pOY012 and pOY009 plasmid electroporations were performed using E. coli NM522 competent cells at 1·4 V, whereas pOY9micF, pOY9ompF and pOY9ompC plasmid electroporations were performed using S. marcescens UOC-67 competent cells at 1·5 V. M9 minimal medium containing M9 salts, 0·1 mM calcium chloride, 0·002 M magnesium sulfate, 20 µg vitamin B1 ml–1, 0·4 % (w/v) glucose, and 100 µg ampicillin ml–1 was used for all strains. M9 salts, vitamin B1, ampicillin, salicylate, glucose, sucrose and ONPG were all obtained from Sigma-Aldrich.
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-galactosidase assays.. Fig. 1 shows the promoter region sequences of ompC and ompF genes in both S. marcescens and E. coli. The promoter region of the S. marcescens ompF gene (GenBank accession no. U81967) was cloned as a 0·5 kb XbaI, genomic DNA, PCR product into the broad-host-range lacZ transcriptional fusion vector pOY009, which harbours the promoterless E. coli lacZ gene (Ozawa et al., 1987). The promoter region of the S. marcescens ompC gene (GenBank accession no. L24960) was cloned as a 0·25 kb XbaI, genomic DNA, PCR product upstream of the promoterless lacZ gene of pOY009, and the micF gene of S. marcescens was cloned as a 0·45 kb XbaI, genomic DNA, PCR product. The orientation of all cloned promoters was confirmed by sequencing and restriction digestion, followed by agarose gel electrophoresis. The induction of the ompC, ompF and micF genes under varying environmental conditions was monitored by assaying for -galactosidase, according to the method of Miller (1972). E. coli NM522, containing pOYL338W, pOY009 and pOY012 lacZ fusion plasmids, and S. marcescens UOC-67, containing pOY9micF, pOY9ompF and pOY9ompC lacZ fusion plasmids, were grown overnight in 3 ml M9 medium containing 0·4 % (w/v) glucose, supplemented with 100 µg ampicillin ml–1, at 37 °C with aeration. Overnight cultures were diluted into fresh M9 medium plus different appropriate experimental additives (sucrose and/or salicylate), and grown to mid-exponential phase, before growth was monitored by measuring OD600. Environmental conditions studied included salicylate concentration (1, 5 and 8 mM), osmotic pressure (5, 8 and 10 % sucrose), pH (pH 6, 7 and 8), and temperature (28, 37 and 42 °C). We decided to experiment at these particular temperatures because S. marcescens strains grow at a minimum temperature of 27 °C, and a maximum temperature of 44 °C (Williams et al., 1971); similar temperature parameters have been used with other enteric bacteria (Dedieu et al., 2002). External pH was manipulated by adjusting the pH of M9 medium containing 0·4 % (w/v) glucose with HCl (pH 6) or 1 M NaOH (pH 8), prior to monitoring the cell growth at OD600. Assays were conducted for each of the single conditions, followed by combining two of the conditions, and then combinations of three conditions. When OD600 reached 0·50, 0·1 ml of each culture was diluted to 1·0 ml with Z buffer (0·06 M Na2HPO4.7H2O, 0·04 M NaH2PO4.H2O, 0·01 M KCl, 0·001 M MgSO4.7H2O, 0·05 M -mercaptoethanol, pH 7·0). Bacterial membranes were disrupted by the addition of one drop of toluene to release -galactosidase into the medium. The -galactosidase reaction was initiated by adding 0·2 ml ONPG (4 mg ml–1), and terminated by adding 0·5 ml 1 M Na2CO3. Enzyme activity was measured by determining absorbance of the o-nitrophenol product (420 nm). Units of -galactosidase activity were calculated according to Miller (1972).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). The highest concentration of sucrose (10 %, w/v) led to a 34 % decrease in expression of the ompF, and a 50 % increase in ompC expression. These findings are consistent with the results of an earlier study on osmoregulation of S. marcescens porins (Hutsul, 1996), and the same pattern holds true for E. coli ompF (pOY012) and ompC (pOYL338W). Considering that bacteria are faced with more than one type of a cellular stressor at a time, the maximum concentration of sucrose was tested in combination with low (28 °C) and high (42 °C) growth temperatures (Table 2). Temperature was found to have a predominant effect over sucrose. When the highest concentration of sucrose (10 %, w/v) was tested in conjunction with pH, it was found that the effect of pH was predominant. In combinations of sucrose, salicylate and temperature, and sucrose, pH and temperature, the temperature effect predominated (Table 2).
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); this is in sharp contrast with the porin studies in E. coli, where the MicF system plays a major role in the negative osmoregulation of ompF in cells grown in media of low-to-intermediate osmolarity (Ramani & Boakye, 2001).
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). At 5 mM salicylate, the expression of ompC increased by approximately 34 %, and the ompF expression was reduced by 25 %. There was a 45 % decrease in the expression of E. coli ompF (pOY012). The addition of 1 mM salicylate, which is the therapeutic concentration most often used (Berlanga & Vinas, 2000), resulted in a 10 % decrease in S. marcescens ompF expression, and a 20 % increase in ompC expression. When salicylate + temperature combinations were examined, temperature was the predominant effect (Table 2). When the highest concentration of salicylate (8 mM) was tested in conjunction with pH, pH was the predominant effect (medium pH was adjusted after the addition of salicylate). Temperature was the prevalent condition when salicylate, temperature and pH combinations were tested, and this was also the case with salicylate, temperature and sucrose (Table 2).
When the effect of salicylate on the S. marcescens micF expression was examined, 1 mM increased the transcription of the micF gene by 10 %, whereas 8 mM salicylate induced the gene by 30 % (Fig. 3b).
Influence of temperature on ompF, ompC and micF expression
When compared with expression of S. marcescens ompF (pOY9ompF) at 28 °C, there was approximately a 55 % decrease in expression at 42 °C. S. marcescens ompC (pOY9ompC) expression was increased by more than 75 % at 42 °C, as compared with 28 °C (Fig. 2c). In the case of E. coli, ompF expression at 42 °C was reduced by 50 % (pOY012), and the expression of ompC increased by 80 % at 42 °C (pOYL338W). In all two- and three-condition assays, the effect of temperature was predominant (Table 2). With respect to micF, transcription increased by approximately 64 % at 42 °C, as compared with 28 °C (Fig. 3c).
Influence of pH on ompF, ompC and micF expression
There was a 30 % increase in the S. marcescens ompC (pOY9ompC) expression in response to acidification of the medium (pH 6), while expression decreased by more than 55 % at pH 8 (Fig. 2d). This finding is consistent with an E. coli study where a 30 % increase in ompC expression was observed at lower pH (Thomas & Booth, 1992), and this was confirmed in the present study using pOYL338W. The opposite trend occurred for S. marcescens ompF (pOY9ompF), where at pH 8, the expression from the ompF promoter was approximately twice as much as that at pH 6. S. marcescens micF expression was similar to ompC expression, such that as pH increased, the production of micF decreased (Fig. 3d).
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DISCUSSION |
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; Cai & Inouye, 2002; Matsubara et al., 2000; Pratt et al., 1996). Our previous investigation revealed that the upstream nucleotide sequence of the cloned S. marcescens ompF gene closely resembles that of E. coli ompF (Hutsul, 1996). However, the OBS and IHF recognition sequences, which are important for repression of ompF transcription by the OmpR–EnvZ regulatory system, are absent in S. marcescens (Fig. 1). This suggests that osmoregulation via this system, as it is described in E. coli, probably cannot take place in S. marcescens.
In addition, we found no change in the transcription of the S. marcescens micF gene in the presence of 5, 8 or 10 % sucrose. This finding is in sharp contrast to an E. coli study that reported a fivefold increase in the level of micF RNA under high osmolarity (Delihas, 1995). Research on the involvement of micF in the osmoregulation of porin genes has yielded contradicting results. One study reported that micF plays a major role in the negative osmoregulation of porin genes in cells grown in media of low-to-intermediate osmolarity (Ramani et al., 1994); however, those experiments were performed at a temperature that stimulates micF transcription by tenfold, and, as such, the effects observed may not be directly related to osmoregulation. Another E. coli study concluded that the micF gene does not play a critical role in osmoregulation, after the authors witnessed a normal level of ompF regulation in a micF mutant strain (Matsuyama & Mizushima, 1985).
We propose that another regulatory system must be involved in the osmoregulation of S. marcescens ompF and ompC porin genes. As demonstrated in this study, S. marcescens regulates the synthesis of the OmpF and OmpC proteins with very strict control under stressful circumstances that greatly mimic their natural environment. Two hypotheses may be able to explain how this regulation is achieved. The first is that a change in the nucleotide sequence in the Pribnow box region occurs, which results in complete osmoregulation (Aiba et al., 1987). E. coli ompF promoters with four different bases at the first position of the Pribnow box were compared for their activity, and it was found that an A to T substitution of the first base resulted in a sharp reduction in ompF expression (Ozawa et al., 1987). The second hypothesis is that higher osmotic pressure increases the degree of negative DNA supercoiling, which could then act to promote ompC gene expression, since changes in DNA supercoiling are synergistic with the changes in OmpR-P in eliciting ompC expression (Graeme-Cook et al., 1989; Hulton et al., 1990). However, the exact mechanism by which osmotic stress can influence the degree of negative supercoiling has not been determined. It is likely that changes in the cytoplasmic concentrations of sucrose molecules are the intermediary effectors (Thomas & Booth, 1992).
Salicylate, being a weak acid, triggers an increased transcription of E. coli ompC and micF, while it leads to a concomitant decrease in OmpF production (Pratt et al., 1996). Addition of higher concentrations of salicylate would lead to an increase in the threshold levels of 4·5S micF RNA available for binding to ompF RNA (Andersen & Delihas, 1990), thereby causing a reduction in the expression of ompF. Similarly, in this study, we found that all of the concentrations of salicylate reduced S. marcescens ompF expression, and increased the expression of S. marcescens ompC (Fig. 2b). An increase in S. marcescens micF expression was also observed in cells grown with 1, 5 and 8 mM salicylate. Therefore, we find that, unlike osmolarity, salicylate strongly blocks the transcription of ompF by increasing the levels of micF. It is not surprising that ompC and micF are similarly regulated by salicylate in S. marcescens, since common OmpR-binding sequences are present in both transcriptional control regions (Hutsul, 1996).
Elevated temperature is another stimulus that increased the levels of S. marcescens micF and ompC mRNA, and decreased the levels of ompF. Unlike the findings for changes in osmolarity, we propose that most of the effect on ompF repression with temperature increase is due to micF. Specifically, MicF would be involved in the post-transcriptional negative regulation of ompF, similar to that in E. coli. In E. coli, the micF RNA forms a stable duplex with the RBS of ompF mRNA, thereby inhibiting ompF translation, and destabilizing the mRNA. OmpF porin production presumably decreases with temperature increase, and, considering that OmpF has wider pores, this would protect S. marcescens from bile salts and other toxic compounds in the intestinal tract.
S. marcescens ompC and micF transcription are both induced by growth of cells in acidic pH conditions. Transcription of micF increased by 63 % at pH 6, as compared with pH 8 (Fig. 3d). In E. coli, this environmental factor represses OmpF production through the EnvZ–OmpR system (Nikaido, 2003). In S. marcescens, the OBS recognition sequences are absent, and thus we propose that the effect of OmpF repression in acidic environments is due to micF. Having an increased synthesis of the narrower-channelled OmpC porins in an acidic environment may contribute to the retention of buffer molecules, such as 
-aminobutyrate, in the periplasm (Nikaido, 2003).
Our initial assumption was that there would be a synergy between different conditions; however, this was not necessarily the case. When cells were grown in the presence of a combination of conditions, such as 28 °C + 10 % sucrose, 28 °C + 8 mM salicylate, 28 °C + 10 % sucrose + 8 mM salicylate, 28 °C + pH 6 + 10 % sucrose, and 28 °C + 8 mM salicylate + pH 6, the effect of growth temperature overpowered the effects of high osmolarity, presence of salicylate and acid pH (Table 2). In these conditions, because the lower temperature of 28 °C is a favourable condition for the expression of ompF porin, the effect of more detrimental conditions, such as the maximum concentrations of salicylate and sucrose, and an acidic pH, seemed to have little influence. A favourable temperature of 28 °C, and presence of stressors, such as salicylate and sucrose, were compensated for by the reduction in the normal pore size of OmpF. In an E. coli study by Zhang & Ferenci (1999), when lactose was used as the sole carbon source in a minimal medium, strains emerged with mutations that altered the residues in the constriction region, or that resulted in a short deletion in the channel-constricting loop L3 of OmpF. We suggest that mutations may have occurred in the PEFGG motif within loop L3, changing it to PEFDG, which would reduce the calculated 1·1 nm OmpF pore size. As such, these strains would produce OmpF porins with a much narrower channel, and demonstrate reduced sucrose or salicylate uptake. S. marcescens ompC has been sequenced (Hutsul, 1996), and it was found that the PEFGG motif conserved within enterobacterial porins is not conserved in the S. marcescens OmpC porin, where it is replaced with the sequence PEFDG. Through liposome-swelling assays (Nikaido et al., 1991), we have determined that the aspartic acid residue (D) at position 112 reduces diffusion of sucrose molecules through loop L3 (Hutsul, 1996). We are currently undertaking liposome-swelling assays using site-specifically altered OmpC to determine if the D residue at position 112 of OmpC also reduces diffusion of salicylate molecules through loop L3. We suggest the possibility exists that such strains would have a reduced OmpC pore channel (<1·0 nm), such that the positive effects of sucrose and salicylate are negligible, and there is an overall decrease in the expression of ompC at 28 °C. At 42 °C, mutations might have occurred in the PEFDG motif within OmpC loop L3, changing it to the PEFGG consensus sequence. Hence, these strains would produce OmpC porins with a wider channel, and would demonstrate increased sucrose and salicylate uptake at 42 °C, and an overall increase in the expression of ompC at 42 °C. In assays where a combination of parameters was examined, with the exception of temperature, basic pH was the predominating factor for the expression of ompF, even in the presence of more detrimental conditions, such as 10 % sucrose and 8 mM salicylate. Again, we propose that possibly there has been a reduction in the pore size of OmpF in order to ‘keep out’ sucrose and salicylate, in the same fashion as explained by Zhang & Ferenci (1999).
In summary, we report that S. marcescens outer membrane porins exhibit regulation in response to osmotic pressure, salicylate, temperature and pH variability. The micF system is one of the main regulatory mechanisms responsible for controlling the expression of OmpF and OmpC porins under all the environmental conditions tested here, with the exception of osmotic shock. In addition, from our multi-condition analyses, we conclude that temperature is the predominant effector, followed by pH. We propose that this finding is due to a reduction and an increase in the pore sizes of OmpF and OmpC porins, respectively.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 10 August 2005;
revised 25 October 2005;
accepted 31 October 2005.
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