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Journal of Bacteriology, August 2005, p. 5831-5836, Vol. 187, No. 16
0021-9193/05/$08.00+0     doi:10.1128/JB.187.16.5831-5836.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Important Role for Methionine Sulfoxide Reductase in the Oxidative Stress Response of Xanthomonas campestris pv. phaseoli

Paiboon Vattanaviboon,1* Chotirote Seeanukun,2 Wirongrong Whangsuk,1 Supa Utamapongchai,1 and Skorn Mongkolsuk1,2*

Laboratory of Biotechnology, Chulabhorn Research Institute, Lak Si, Bangkok 10210,1 Department of Biotechnology, Faculty of Science, Mahidol University, Bangkok 10400, Thailand2

Received 18 February 2005/ Accepted 1 June 2005


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ABSTRACT
 
A methionine sulfoxide reductase gene (msrA) from Xanthomonas campestris pv. phaseoli has unique expression patterns and physiological function. msrA expression is growth dependent and is highly induced by exposure to oxidants and N-ethylmaleimide in an OxyR- and OhrR-independent manner. An msrA mutant showed increased sensitivity to oxidants but only during stationary phase.


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TEXT
 
Xanthomonas spp. are soil bacteria that are the causative agents of bacterial blight diseases in many economically important crops. Bacteria are constantly exposed to harmful reactive oxygen species (ROS) that originate from many sources, such as aerobic respiration, chemical pollutants in the environment, and the initial defense responses of plants to microbial invasion. ROS are highly reactive and can damage biological macromolecules, including proteins, nucleic acids, and lipids. Methionine residues in proteins are particularly susceptible to oxidation by ROS resulting in formation of racemic mixtures of methionine-S-sulfoxide and methionine-R-sulfoxide. Most eukaryotic and prokaryotic cells possess repair enzymes, such as peptide methionine sulfoxide reductases (Msr proteins), which catalyze the thioredoxin-dependent reduction of either free methionine sulfoxide [Met(O)] or protein-bound Met(O) to methionine. Escherichia coli and several other bacteria have two methionine sulfoxide reductases, namely, MsrA and MsrB, encoded by two structurally unrelated genes (20). MsrA and MsrB have distinct substrate specificities. MsrA uses only the S epimer, while MsrB uses the R epimer of Met(O) as a substrate (6, 17).

In bacteria, the physiological function of the Msr proteins has not been fully elucidated. In general, msrA is recognized as a gene required for bacterial virulence and survival under some stressful conditions (4, 18, 20). Examination of msrA expression patterns could give important clues as to its physiological function(s). While different bacteria appear to display different msrA expression patterns in response to various conditions, in no case has a regulator of msrA expression been identified. Moreover, there is little correlation between the gene expression pattern and any possible physiological role for the gene. For example, MsrA has been shown to play a significant role in the protection of several microorganisms from oxidative stress, and yet in none of these bacteria has the gene been shown to be oxidative stress inducible (5, 18-20, 22, 26). In many microorganisms, the mechanism of regulation of msrA expression and the physiological function(s) of the gene product remain to be elucidated.

In this paper, the expression patterns of msrA in Xanthomonas campestris pv. phaseoli were examined. The gene has novel patterns of growth-phase-dependent and oxidative-stress-inducible expression. The oxidative-stress-inducible expression of msrA is not regulated by known stress sensors and transcriptional regulators. Physiological analysis of an msrA mutant indicated that the gene plays an important role in the protection against oxidative stress.

Nucleotide sequence accession number. The nucleotide sequence determined in this study was assigned GenBank accession number AF404824.

Cloning, genome organization, and transcription of the msrA locus from X. campestris pv. phaseoli. The isolation of a genomic clone (pA301) containing talA, encoding a transaldolase, from X. campestris pv. phaseoli was reported previously (24). Analysis of the nucleotide sequence downstream of talA revealed the presence of an unidentified open reading frame (ORF) and a truncated ORF with high homology to the C-terminal region of MsrA. A fragment containing this truncated gene (0.45-kb SphI fragment from pA301) was used as a probe to isolate a DNA fragment containing full-length msrA from an existing genomic library constructed in {lambda}Zip-lox (11). A positively hybridizing plaque was purified and excised into plasmid pA8. Analysis of the nucleotide sequence revealed that the fragment contained the putative msrA that was predicted to encode a 216-amino-acid polypeptide with a molecular mass of 23.5 kDa and a pI of 5.39. The deduced amino acid sequence of Xanthomonas MsrA showed a high degree of identity to both eukaryotic and prokaryotic peptide methionine sulfoxide reductases (MsrA). Analysis of the Xanthomonas MsrA amino acid sequence showed the presence of a conserved consensus sequence, GCFWG, that is thought to comprise the active site of the enzyme (17), and two cysteine residues at the C terminus which correspond to Cys-198 and Cys-206 of E. coli MsrA that have been shown to be involved in catalysis (17, 23).

msrA was located between two ORFs of unknown function (orfXA and orfXB) on the X. campestris pv. phaseoli genome (Fig. 1A). Nonetheless, the genes in this region showed an interesting organization. Comparison of the sequence of the msrA region of X. campestris pv. phaseoli with those of X. campestris pv. campestris and Xanthomonas axonopodis pv. citri showed that the gene organization hemK-ahpC-ahpF-oxyR-orfX1-rnk-talA-orfXA-msrA-orfXB (Fig. 1A) was conserved among the three bacteria (2). msrA is located in a region rich in genes involved in the oxidative stress response. We have shown that, in addition to msrA, ahpC and ahpF, encoding the catalytic and the reductase subunits of alkyl hydroperoxide reductase, respectively, and the peroxide sensor and transcription regulator OxyR are essential for the peroxide stress protection response (10, 13). Moreover, talA also plays an important role in protecting the bacteria from a superoxide generator, menadione (MD) (24).



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  		FIG. 1. Gene organization and growth-phase-dependent expression of msrA. (A) Physical and transcription maps of msrA in X. campestris pv. phaseoli. The arrows indicate the orientations and lengths of the transcripts. Question marks indicate uncharacterized genes. (B) Results of a Northern blot hybridization showing msrA expression at different growth phases. At the indicated times, RNA samples were prepared from cultures of X. campestris pv. phaseoli. RNA isolation, gel electrophoresis, and Northern blotting were done as previously described (15). Ten micrograms of total RNA was loaded into each lane. The blot was probed with a radioactively labeled msrA fragment (15). (C) Growth curve and expression analysis of X. campestris pv. phaseoli strain Xp08 containing an msrA promoter-lacZ fusion. The growth curve ({circ}) of Xp08 (msrA::lacZ) in SB medium was determined at 28°C with continuous shaking at 150 rpm. At the indicated times, samples were removed and crude lysates were prepared and assayed for ß-galactosidase activity (14). OD600, optical density at 600 nm.

A partial transcription map of the region is also shown (Fig. 1A). The transcripts encoding ahpC, ahpF-oxyR-orfX1, and talA have been previously determined (13, 24). Northern analysis, using a 340-bp SmaI-SphI msrA-specific fragment as a probe, indicated that msrA was transcribed on a 0.7-kb monocistronic mRNA (Fig. 1B).

Growth-phase-dependent expression of msrA. The expression of msrA during the different stages of bacterial growth has not been well studied. In some bacteria, msrA appears to play important roles in oxidative stress protection (4, 18, 20, 26). Hence, the timing of its expression is likely to be important, since the levels of resistance to oxidative stress vary significantly at different stages of growth (11). The growth-phase-dependent expression patterns of msrA were investigated by use of both Northern blot analysis and msrA promoter-lacZ fusion analysis. The results of Northern hybridizations showed that msrA was expressed at low levels during exponential-phase growth (Fig. 1B). The expression increased eightfold (as judged by densitometer analysis of Northern blots) as the culture entered the stationary phase and during the stationary phase. These results were independently confirmed by use of an msrA promoter-lacZ fusion construct. A promoterless lacZ was transcriptionally fused to msrA on the X. campestris pv. phaseoli chromosome (msrA::lacZ) to yield strain Xp08 by using the R6K-derived suicide plasmid pVIK112 (7) inserted with the 273-bp DNA fragment of the msrA coding region (corresponding to nucleotides 121 to 393) at EcoRI and SmaI sites. The plasmid was introduced into X. campestris pv. phaseoli by electroporation. Xp08 was selected by its kanamycin resistance and was confirmed by Southern blot analysis (data not shown). msrA promoter activity (ß-galactosidase activity) was monitored in Xp08 throughout the different growth phases. As shown in Fig. 1C, the ß-galactosidase activity increased twofold (from 30 to 60 U mg–1 protein) as growth proceeded from exponential to stationary phase, with peak ß-galactosidase levels being attained as cells entered the stationary phase and during the stationary phase of growth. These results are consistent with those of the Northern hybridization analysis and indicated that the expression of msrA is stationary phase dependent. A similar pattern of msrA expression in E. coli has been observed (18). Generally, soil bacteria spend long periods in a nutrient-limited state and have evolved mechanisms to survive under starvation conditions that involve increasing the expression of genes that protect them from the various starvation-associated stresses (21). The growth-phase-dependent expression pattern of msrA suggests that it belongs to the starvation stress response genes. msrA is likely to play an important physiological role(s) during stationary phase. The mechanism(s) controlling stationary-phase-dependent gene expression in Xanthomonas is not known; analysis of the bacterial genome did not show any ORFs with high homology to RpoS, suggesting that other sigma factors or additional regulatory mechanisms may control stationary-phase-dependent msrA expression. Interestingly, the regulator of stationary-phase expression of E. coli msrA is also not known, but it has been shown that the regulator is not {sigma}S (18).

Oxidative stress induction of msrA expression. In several bacteria, msrA has been shown to be important in protecting bacteria from oxidative stress, probably by repairing oxidized Met residues (27). However, in the bacteria thus far investigated, msrA expression has not been shown to be induced by oxidative stress (5). This suggests that the constitutive basal expression of msrA is sufficient to confer protection against oxidative stress generated from internal and external sources. In X. campestris pv. phaseoli, as in other bacteria, exposure to sublethal levels of oxidants leads to a severalfold increase in the expression of oxidative-stress-protective enzymes, such as catalase (KatA), alkyl hydroperoxide reductase (AhpC), and organic hydroperoxide resistance thiol peroxidase (Ohr) (1, 13, 15). This inducible response plays an important role in protecting the bacterium against stresses. Thus, msrA expression in response to exposure to various oxidants was investigated by Northern blot analysis. Exponential-phase cultures of X. campestris pv. phaseoli grown in SB medium (15) were treated with N-ethylmaleimide (NEM), H2O2, MD, or tert-butyl hydroperoxide (tBOOH) for 10 min. RNA samples were extracted (15) and analyzed by Northern blot hybridization using a radioactively labeled msrA probe. The results in Fig. 2A show that pretreatment of the cultures with MD induced msrA expression 10-fold, while tBOOH, H2O2, and NEM pretreatments produced intermediate levels of induction of sixfold, threefold, and twofold, respectively. The oxidant induction of msrA promoter was done using an msrA promoter-lacZ fusion. A similar pattern of oxidant induction of msrA promoter was obtained in Xp08 (msrA::lacZ), with menadione being the most potent inducer, followed by H2O2, tBOOH, and NEM (Fig. 2D). In Xanthomonas, MD, H2O2, and tBOOH have all been shown to be potent inducers of genes in the OxyR regulon, while tBOOH also induces genes in the OhrR regulon (13, 15). NEM induction of msrA probably results from the depletion of thiol antioxidant molecules and the inactivation of oxidant scavenging enzymes that lead to oxidative stress. The observed pattern of oxidant-inducible msrA expression in Xanthomonas differs from previous reports of other bacteria, in which induction of msrA expression has been observed in response to a shift in pH (26), exposure to phenolic compounds (22), and treatment with cell wall-active antibiotics but not to oxidative stress (19).



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  		FIG. 2. Oxidant-inducible msrA expression and localization of the msrA promoter. X. campestris pv. phaseoli exponential-phase cultures were treated with 100 µM NEM, 200 µM H2O2, 200 µM MD, or 200 µM tBOOH for 10 min before total RNA was isolated, and Northern blots were prepared and probed with a radioactively labeled msrA-specific probe. Ten micrograms of total RNA was loaded into each lane in all Northern blot hybridization experiments. (A) Northern blot showing msrA expression in response to oxidant treatments in X. campestris pv. phaseoli (Xp). The arrow indicates the size of the msrA mRNA. Un, uninduced. (B) Northern blots of msrA expression in response to various concentrations of H2O2. (C) Northern blot showing msrA expression in X. campestris pv. phaseoli oxyR and ohrR mutants treated with various oxidants. The ohrR and oxyR mutants were grown and treated with oxidants as described for panel A with the exception that the oxyR mutant was treated with 100 µM H2O2, 100 µM MD, or 100 µM tBOOH. (D) Xp08 (msrA-lacZ) was grown and treated with various oxidants. Crude lysate preparation and ß-galactosidase levels were determined as previously described (14). (E) Primer extension of RNA extracted from uninduced (Un) and MD-induced cultures. The experiment was performed using 32P-labeled oligonucleotide primer BT110 (5'CTAACGTTGTTTGAAGGCG3') as previously described. C, T, A, and G are sequence ladders generated by using the same primer. The arrowhead indicates the msrA transcription start site. Putative –35 and –10 regions are shown in bold, capital letters. A putative ribosome binding site (rbs) is marked in bold, lowercase letters, and the translation initiation codon ATG is in bold italics.

Since X. campestris pv. phaseoli msrA displayed a unique oxidant-inducible expression pattern, we attempted to identify the regulator involved in controlling the expression of the gene. The oxidant-inducible expression pattern of msrA was similar to the patterns observed for many OxyR-regulated genes (10, 12). In Xanthomonas, OxyR is a peroxide sensor and a global transcriptional regulator of peroxide stress and OxyR-regulated genes are involved in the detoxification of H2O2 (katA) and organic hydroperoxides (ahpC) (1, 10, 13). Thus, analyses of the effects of oxidants on the expression of msrA in the wild type and an oxyR mutant were performed. The results shown in Fig. 2C clearly showed that the pattern of oxidant-induced msrA expression was not affected by inactivation of oxyR, since msrA transcription was highly induced by tBOOH. It should be noted that the inducing concentrations of oxidants were lowered to 100 µM for H2O2, MD, and tBOOH and 50 µM for NEM due to the oxyR mutant's inherent hypersensitivity to oxidants relative to the wild type (16). The effect of inactivation of the organic-hydroperoxide-sensing transcription repressor, ohrR, on msrA expression was also tested (14). The results of Northern blot analyses using the parental strain and an ohrR mutant showed that the profiles of oxidant induction of msrA in the two strains were similar (Fig. 2A and C). From these results, we concluded that both oxyR and ohrR are not responsible for the regulation of msrA expression. The evidence suggests the existence of an unidentified regulator(s) that could sense and respond to oxidative stress by increasing transcription of msrA.

The relative levels of peroxide induction in the wild type and oxyR and ohrR mutants reveal interesting patterns. The magnitude of H2O2 and tBOOH induction of msrA was lower in the parental strain than in either the oxyR or ohr mutant strain (Fig. 2B and C). This is due to the inability of the oxyR mutant to induce expression of the catalase and alkyl hydroperoxide reductase genes, which are responsible for H2O2 and organic hydroperoxide detoxification, respectively. Similarly, the ohrR mutant that has decreased ohr expression due to a polar effect of the mutation in ohrR (14) thus has a reduced capacity to metabolize organic hydroperoxide. Thus, in the regulatory mutants, intracellular peroxide levels were higher due to lower levels of peroxide detoxification enzymes. This would result in increased protein oxidation in the mutants relative to the parental strain, which in turn may stimulate higher levels of msrA induction. At present, the regulator(s) of oxidant-induced msrA expression has not been identified, and it remains to be seen whether such a regulator directly or indirectly senses oxidants and/or oxidized proteins.

In order to localize the msrA promoter region, the transcription initiation sites of msrA mRNA, isolated from uninduced and MD-induced cultures, were mapped by primer extension. The results shown in Fig. 2E showed a single predominant primer extension product corresponding to a transcription initiation site located 27 nucleotides upstream of the msrA translation start. Analysis of the sequence upstream of the transcription start site revealed the presence of a –10 promoter sequence, TTGAAA, separated by 17 nucleotides from a –35 promoter sequence, CATCCA. The msrA promoter –35 and –10 regions matched the consensus sequences for X. campestris promoters at 6/6 and 4/6 nucleotides, respectively (8). No sequences similar to the consensus binding sites for either OxyR or OhrR were found in the vicinity of the msrA transcription start. This was consistent with the results of the Northern blot analyses that indicated that OxyR and OhrR are not involved in the regulation of msrA. In addition, the primer extension results clearly showed that MD pretreatment increased msrA transcription initiation (Fig. 2E). Thus, the increase in the steady-state level of msrA mRNA after MD treatment is at least in part due to increased transcription of msrA.

Analysis of the physiological role of msrA. As mentioned previously, the physiological roles of msrA appear to differ in different bacteria. In order to determine the physiological role of msrA in X. campestris pv. phaseoli, an msrA-disrupted mutant was constructed by insertional inactivation using the nonreplicative plasmid pKStet (a tetracycline resistance derivative of pBluescript KSII [Stratagene]) containing a 220-bp internal fragment of msrA. The msrA mutant strain Xp07 was isolated, and the insertional inactivation of the gene was confirmed by both PCR and Southern blot analysis (data not shown). First, the aerobic growth rates of the mutant and the parental wild-type strain were determined in complex medium (Silva Buddenhagen [SB]) and minimal medium (M9). No significant difference between the growth rates of the strains was observed (data not shown). Thus, the loss of msrA function caused no adverse effects on bacterial growth. Recent reports suggested that in some bacteria, inactivation of msrA led to increased sensitivity to oxidative stress, indicating the importance of the gene in protecting bacteria from the stress. The level of resistance of the msrA mutant against various oxidants was determined as previously described (3) and compared with that of the parental strain. Exponential- and stationary-phase cultures were serially diluted and overlaid on SB agar plates containing the appropriate concentrations of oxidants, including H2O2, tBOOH, MD, and NEM. The surviving colonies were counted after 48 h of incubation at 28°C. During exponential-phase growth, Xp07 and the parental strain had similar levels of resistance to all oxidants tested (Fig. 3A). However, high-level expression of msrA from the plasmid pMsrA (broad-host-range plasmid pBBR1MCS-2 [9] containing the msrA gene) in Xp07 resulted in a small (7- to 10-fold) increase in the levels of resistance to H2O2, tBOOH, and NEM (Fig. 3A) relative to those of the parental strain. This observation suggested that the enzyme does not play a major role in protecting X. campestris pv. phaseoli from oxidant killing during the exponential phase of growth. Nonetheless, high-level expression of msrA does provide additional protection against oxidant killing.



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  		FIG. 3. Determination of oxidant resistance levels in X. campestris pv. phaseoli strains. Xanthomonas strains were grown in SB medium for 4 h for exponential-phase experiments and 30 h for stationary-phase experiments. Determination of oxidant resistance levels was done using a plate sensitivity assay as previously described (3) with some modifications. Essentially, cell aliquots were serially diluted in 50 mM sodium phosphate buffer, pH 7.0, prior to being plated on SB agar alone and SB agar containing the indicated concentration of oxidants. The colonies were scored after incubation at 28°C for 48 h. The surviving fraction was defined as the number of CFU from the oxidant-containing plate divided by the number of CFU from the SB agar plate. Experiments were repeated three times, and means and standard deviations are shown. The survival curves of the msrA mutant (Xp07 [•]), Xp07 harboring pMsrA ({square}), and the parental wild type ({circ}) are shown.

Analysis of growth-phase-dependent oxidant resistance levels indicated that msrA played an important protective role against oxidant killing during the stationary phase of growth. The stationary-phase cells of msrA mutant strain Xp07 were 10- to 100-fold more sensitive to H2O2, tBOOH, MD, and NEM treatments than the parental strain (Fig. 3B), and the oxidant sensitivity phenotype of Xp07 could be complemented by pMsrA. Analysis of related X. campestris pv. campestris genome has shown the existence of msrB. The phenotypes of msrA mutant could not be complemented by expression of msrB in an expression vector (data not shown).

In Xanthomonas, as well as in other bacteria, stationary-phase cells are highly resistant to oxidant killing (11). The mechanisms responsible for stationary-phase resistance to oxidants are not fully understood but are thought to be independent of the levels of scavenging enzymes. It has been previously shown that the activities of oxidant-scavenging enzymes, such as catalase and superoxide dismutase, decreased as Xanthomonas cultures entered into the stationary phase and during the stationary phase of growth (11, 25). This is likely to lead to intracellular accumulation of oxidants and a subsequent increase in the oxidation of macromolecules. Thus, during stationary phase, enzymes that are involved in the various repair processes, such as MsrA, become important in protecting cells from intracellular oxidants. Xanthomonas msrA is the only protein oxidation repair system thus far studied that shows a good correlation between the gene expression pattern and its physiological role. During normal growth, exponential-phase cells are less likely to be damaged by oxidants, due to the presence of high levels of oxidant-scavenging enzymes. However, during exponential phase, the bacteria are still highly susceptible to extracellular oxidants. The oxidant-inducible expression of msrA during exponential phase provides the cells with additional MsrA to repair damage caused by exposure to extracellular oxidants. This is reflected in the low level of msrA expression during exponential phase. As growth continues into stationary phase, a decline in scavenging enzyme activities (11, 25) leads to an increase in the intracellular accumulation of oxidants and hence the need to increase msrA expression to repair oxidized proteins.


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ACKNOWLEDGMENTS
 
We thank J. M. Dubbs for a critical reading of the manuscript.

This research was supported by a Research Team Strengthening Grant from the BIOTEC, by Senior Research Scholar Grant RTA4580010 from the Thailand Research Fund to S.M. and by grants from the ESTM through the Higher Education Development Project of the Commission on Higher Education, Ministry of Education.


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FOOTNOTES
 
* Corresponding author. Mailing address: Laboratory of Biotechnology, Chulabhorn Research Institute, Lak Si, Bangkok 10210, Thailand. Phone: 66 2574 0630, ext. 3816. Fax: 66 2574 2027. E-mail for P. Vattanaviboon: paiboon{at}cri.or.th. E-mail for S. Mongkolsuk: skorn{at}cri.or.th. Back


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Journal of Bacteriology, August 2005, p. 5831-5836, Vol. 187, No. 16
0021-9193/05/$08.00+0     doi:10.1128/JB.187.16.5831-5836.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Atack, J. M., Kelly, D. J. (2008). Contribution of the stereospecific methionine sulphoxide reductases MsrA and MsrB to oxidative and nitrosative stress resistance in the food-borne pathogen Campylobacter jejuni. Microbiology 154: 2219-2230 [Abstract] [Full Text]  

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