An extracytoplasmic function sigma factor-dependent periplasmic glutathione peroxidase is involved in oxidative stress response of Shewanella oneidensis
© Dai et al.; licensee BioMed Central. 2015
Received: 8 July 2014
Accepted: 20 January 2015
Published: 18 February 2015
Bacteria use alternative sigma factors (σs) to regulate condition-specific gene expression for survival and Shewanella harbors multiple ECF (extracytoplasmic function) σ genes and cognate anti-sigma factor genes. Here we comparatively analyzed two of the rpoE-like operons in the strain MR-1: rpoE-rseA-rseB-rseC and rpoE2-chrR.
RpoE was important for bacterial growth at low and high temperatures, in the minimal medium, and high salinity. The degP/htrA orthologue, required for growth of Escherichia coli and Pseudomonas aeruginosa at high temperature, is absent in Shewanella, while the degQ gene is RpoE-regulated and is required for bacterial growth at high temperature. RpoE2 was essential for the optimal growth in oxidative stress conditions because the rpoE2 mutant was sensitive to hydrogen peroxide and paraquat. The operon encoding a ferrochelatase paralogue (HemH2) and a periplasmic glutathione peroxidase (PgpD) was identified as RpoE2-dependent. PgpD exhibited higher activities and played a more important role in the oxidative stress responses than the cytoplasmic glutathione peroxidase CgpD under tested conditions. The rpoE2-chrR operon and the identified regulon genes, including pgpD and hemH2, are coincidently absent in several psychrophilic and/or deep-sea Shewanella strains.
In S. oneidensis MR-1, the RpoE-dependent degQ gene is required for optimal growth under high temperature. The rpoE2 and RpoE2-dependent pgpD gene encoding a periplasmic glutathione peroxidase are involved in oxidative stress responses. But rpoE2 is not required for bacterial growth at low temperature and it even affected bacterial growth under salt stress, indicating that there is a tradeoff between the salt resistance and RpoE2-mediated oxidative stress responses.
The γ-proteobacteria Shewanella species have two hallmark traits, respiratory versatility and psychrophily [1,2]. Respiratory versatility is characterized by their ability to utilize a series of organic and inorganic electron acceptors, particularly metals and metalloids of Fe(III), Mn(IV), Ur(VI) and the direct electron transfer to electrodes [3,4]. Shewanella species harbor a variety of outer membrane and periplasmic c-type cytochrome genes expressed for respiration under different environmental conditions. Bacterial gene expression is regulated by a series of transcriptional factors including alternative sigma factors (σS). Sigma factors are a component of bacterial RNA polymerase (RNAP) and determine promoter selectivity of the holoenzyme, thus playing a central role in the regulation of gene expression. Bacteria usually have one housekeeping σ factor (RpoD) and a variable number of alternative σ factors that possess different promoter-recognition properties . The number of alternative σ factors highly varies among bacteria and may be related to their specific habitat, metabolisms, and development [5-9]. Extracytoplasmic function (ECF) σ factors are highly regulated factors that control expression of genes and constitute the third pillar of bacterial signal transduction after the one-component and two-component systems . Most ECF σs are sequestered by an anti-sigma factor, which can be deactivated by proteolysis, conformational change, partner switching (including mimicry) or other unknown mechanisms to release the ECF sigma factor from being sequestered . Once the ECF sigma factor is released it can then activate of transcription of regulon genes throughout the genome. ECF sigma factor RpoE and its regulators have been extensively studied in E. coli [10-17], Pseudomonas aeruginosa [18-22] and Bacillus subtilis [6,7]. RpoE regulates a series of extracytoplasmic functions, including synthesis of envelope proteins, outer membrane protein (OMP) modification, cell envelope structure and cell division in E. coli . The RpoE counterpart AlgU/T controls the production of a series of pathogenic factors, lipoproteins, and the extracellular polysaccharide alginate in P. aeruginosa which causes the mortality and morbidity of patients with cystic fibrosis [24-26].
The sigma factors of Shewanella have remained relatively uncharacterized. The genome of Shewanella oneidensis MR-1 encodes 10 sigma factors (RpoD, RpoH, RpoS, RpoN, FliA, and five ECF sigma factors RpoE, RpoE2, SO_3551 (ECF-like), SO_3096 (ECF-like) and SO_3840 (ECF-like). Sigma32 (RpoH) is the heat shock response sigma factor and it has been shown that heat shock activates expression of 323 genes and represses expression of 286 genes [27,28]. In S. violacea strain DSS12, three RpoE-like sigma factors have been identified [29,30]. Numerous transcriptomic studies have shown Shewanella can modulate gene expression in response to its environmental signals [29-37]. To shed light on the role of two of the RpoE sigma factors of S. oneidensis MR-1, comparative studies were conducted in this study. Deletion mutants were generated and utilized to ascertain the specific functions of each RpoE sigma factor and the two sigma factors dependent genes were identified. RpoE was required for growth at cold and high temperatures, in minimal media, and in high salt environments. Unlike RpoE, RpoE2 is responsible for resistance to oxidative stress. PgpD was identified as the RpoE2 dependent periplasmic glutathione peroxidase that facilitates resistance to oxidative stress. Understanding the regulation of RpoE and RpoE2 and the genes they control can help explain the ability of S. oneidensis to survive against environmental stress.
RpoE ECF sigma factors and anti-sigma factor genes in S. oneidensis MR-1
RpoE and RpoE2 of S. oneidensis are responsible for diverse stress responses
RpoE is autoreglated and DegQ is RpoE-dependent
Promoter motifs-based prediction of RpoE and RpoE2 regulon members in the genome of Shewanella oneidensis MR-1
Putative RpoE-dependent promoter sequence
Other genes in the operon
FKBP-type peptidyl prolyl cis-trans isomerase
RNA polymerase sigma 24 factor
Outer membrane protein (OMP) assembly complex subunit E
Peptidyl prolyl cis-trans isomerase A
Membrane associated zinc metalloprotease
bamA(SO_1637)-skp(SO_1638)- lpxD(SO_1639)-fabZ(SO_1640)- lpxA(SO_1641)-lpxB(SO_1642)- rnhB(SO_1643)
OMP assembly complex subunit C
OMP assembly complex subunit B
OMP assembly complex subunit D
Lipopolysaccharide (LPS) transporter subunit D
LPS assembly protein
Periplasmic serine protease
LPS transporter (LPT) subunit C
LPS transporter subunit A
Conserved hypothetical protein
RNA polymerase sigma 32 factor
RpoE2-dependent promoter sequence
ECF RNA polymerase
chrR (SO_1985, anti-sigma factor)
Lon domain protease
Periplasmic glutathione peroxidase
hemH2 (SO_3348, ferrochelatase)
Photoreactivation-associated inner membrane protein
phrB (SO_3384, deoxyribo-dipyrimidine photolyase) cfa (SO_3379, cyclopropane fatty acid synthase)
Deoxyribodipyrimidine photolyase-related protein
SO_4170 (CsgA short chain dehydrogenase/reductase)
RpoE2 mediates resistance to oxidative stress responses
Identification of the RpoE2 regulon of S. oneidensis
RpoE2–dependent periplasmic hydrogen peroxidase is involved in oxidative stress response
In light of the fact that RpoE2 plays a role in resistance to oxidative stress, we looked at the RpoE2 regulon for genes that encode proteins that could be responsible. Notably, the RpoE2 regulon member SO_3349 encodes a periplasmic gluthathione peroxidase D (designated pgpD hereafter), which may be required for coping with the oxidative stress in the compartment of periplasm. The pgpD and the downstream hemH paralogue (SO_3348) had not been previously identified as the RpoE-ChrR regulon members in the photosynthetic α-bacterium Rhodobacter sphaeroides. The PhoA-fusion assays  demonstrated that PgpD is secreted into the periplasm as previously predicted because the signal peptide of PgpD could mediate the secretion of PhoA (Additional file 1: Figure S10). We also mapped the transcription start site of the predicted RpoE2 regulon member SO_3349 and it is shown that the transcription of pgpD (SO_3349) does start from the nucleotide A (+1) downstream of the −35 (TGATCC) and −10 (CGTAAT) promoter motifs as it was shown (Additional file 1: Figure S3C and S7). We have generated the in-frame deletion mutants of pgpD and cgpD and tested the sensitivity of the mutants to hydrogen peroxide and paraquat. Our results showed that the pgpD deletion mutant (MR-1ΔpgpD) exhibited a significantly higher sensitivity to oxidative stresses than the MR-1 strain (p < 0.01) while no remarkable difference was observed between the cgpD mutant (MR-1ΔcgpD) and wild-type strain under the tested concentrations (Figure 5). The growth defectiveness of the pgpD deletion mutant in the presence of hydrogen peroxide and paraquat could be rescued by genetic complementation of plasmid borne-pgpD gene (Additional file 1: Figure S11). Though PgpD obviously plays a more important role than CgpD under our tested conditions, the double mutant (MR-1ΔcgpDΔpgpD) was more sensitive to hydrogen peroxide stress than the MR-1ΔrpoE2 and MR-1ΔpgpD single mutants (Figure 5), indicating that the cgpD gene is also involved in oxidative stress responses.
Expression and activity assays of cyptoplasmic and periplasmic hydrogen peroxidases
Absence of RpoE2-ChrR pair and the regulon members in psychrophilic and/or deep-sea strains
The RpoE2-ChrR system and the regulon members of RpoE2 may play a crucial part in coping with environmental stresses such as UVA radiation and more importantly reactive oxygen species (ROS) in Shewanella. The ROS could be sensed by ChrR, which undergoes conformational changes and releases the sequestered RpoE2. The released RpoE2 undergoes auto-upregulation by binding to the promoter of rpoE2-chrR operon and then drives the expression of enzymes involved in modification of cell membrane (Cfa), DNA damage repair (PhrB), degradation of ROS (PgpD) and other stress responses. Our comparative genomic analysis revealed that the rpoE2-chrR operon and these identified RpoE2 regulon member genes (SO_1987, SO_3348-SO_3349, SO_3374-SO_3386, and SO_4169-SO_4170) are coincidently absent in several Shewanella strains, including S. pealean ATCC 700345 , S. sediminis HAW-EB3 , S. piezotolerans WP3 , S. halifaxensis HAW-EB4 , S. violacea DSS12 [29,51], and S. benthica KT99 , which are deep-sea and/or psychrophilic strains .
In this study the cellular functions of two RpoE-ECF sigma factors of S. oneidensis were investigated by comparative genomics, molecular genetics and physiological analyses. We have shown that RpoE is required for bacterial response to a series of stresses, including nutrient depletion (minimal medium), high salinity (3% sodium chloride), high and cold temperatures (33°C and 4°C), and oxidative stresses (hydrogen peroxide and paraquat) in the S. oneidensis MR-1 strain. On the other hand, RpoE2 is only involved in oxidative stress responses.
In E. coli and P. aeruginosa, the rpoE/algU gene is autoregulated because an RpoE/AlgU-dependent promoter is located upstream of this gene [23,24]. RpoE regulates a series of extracytoplasmic functions, including synthesis of envelope proteins, outer membrane protein (OMP) modification, cell envelope structure and cell division in E. coli . The RpoE counterpart AlgU/T controls the production of a series of pathogenic factors, lipoproteins, and the extracellular polysaccharide alginate in P. aeruginosa which causes the mortality and morbidity of patients with cystic fibrosis [24-26]. RpoE is involved in biogenesis of envelope and integrity maintenance as previously demonstrated in mesophilic and psychrophilic bacteria . Our results are consistent with previous microarray analysis data that the rpoE exhibited altered transcription under several stress conditions (summarized in the Additional file 1: Table S4). The N-terminal domain of ChrR of R. sphaeroides is structurally similar to that of RseA of E. coli and defines a common cupin fold among anti-σ factors [44,45].
The Shewanella strains harbor a large number of c-type cytochrome genes for respiration. A total of 32 and 41 c-type cytochrome genes are present in S. putrefaciens W3-18-1 and S. oneidensis MR-1, respectively . These cytochromes and respiratory chains are a potential source of singlet oxygen [44,45], which may account for the presence of the rpoE2-chrR pair and the periplasmic glutathione peroxidase gene pgpD in most of the sequenced Shewanella strains. On the other hand, the rpoE2-chrR pair and the identified regulon members are coincidentally absent in the deep-sea/psychrophilic strains of Shewanella. The deep-sea water is characterized by a very low temperature, typically from 0°C to 3°C, a high salinity of about 3.5%, as well as low radiation. As described above, rpoE2 was not required for bacterial growth under high temperature, nutrient deficiency and particularly cold temperature and high salinity encountered in deep-sea environments. More importantly, the deletion of rpoE2 even enhanced the bacterial growth under salt stress condition (Figure 2E and Additional file 1: Figure S1). On the other hand, overexpression of rpoE2 affected bacterial growth under salt stress condition (Additional file 1: Figure S12). These results indicated a tradeoff between oxidative stress response and salt stress tolerance. The loss of these genes may represent a bacterial adaptation to deep-sea and cold environments of high salinity. It remains intriguing why RpoE2–mediated changes affect the bacterial growth under high salinity. The functions and regulation of other ECF σs remain largely unknown in Shewanella . The signaling mechanism for the activation and regulon of each σ factor need to be experimentally investigated since their functions could not be completely predicted based on the existing knowledge from the closely related bacteria and comparative genomics analyses as shown by our results.
Two of the ECF sigma factors, RpoE and RpoE2, regulate a series of extracytoplasmic functions in S. oneidensis MR-1. It is revealed that the RpoE-dependent degQ gene is required for optimal growth under high temperature. The rpoE2 and RpoE2-dependent pgpD gene are involved in oxidative stress responses. The glutathione peroxidase PgpD is secreted into the periplasm and plays a more important role in oxidative stress responses than the cytoplasmic homlog CgpD. But rpoE2 is not required for bacterial growth at low temperature and it even affected bacterial growth under salt stress, indicating that there is a tradeoff between the salt resistance and RpoE2-mediated oxidative stress responses.
Bacterial strains, plasmids, culture conditions and genome sequences
The bacterial strains and plasmid used in this study were listed in Additional file 1: Table S1. Bacterial strains were usually cultured in Lysogeny Broth (LB) (containing 10 g tryptone, 5 g yeast extract, and 5 g sodium chloride per litre) media/plates and the modified M1 minimum media (50 mM sodium lactate was used as a carbon source. when necessary, supplemented with 15 and 50 μg/ml of gentamycin and kanamycin, respectively) . S. oneidensis MR-1 (ATCC 700550) was isolated from the sediment of Lake Oneida, New York  and usually incubated at 28°C in our laboratory. The whole genome sequences for around 30 strains of Shewanella are available at the NCBI microbial genome database. The genome of S. oneidensis MR-1 was sequenced and annotated by J. Craig Venter Institute  and other strains were analyzed by Joint Genome Institute and other institutions. The geographical origin of Shewanella strains and isolation site characteristics were summarized previously [1,2]. Pseudomonas aeruginosa PAO1 strain was obtained from ATCC (Manassas, VA, USA).
Polypeptide and nucleotide sequences of genes were retrieved from NCBI database by using BLAST searches. The orthologous relationships among the homologous genes from each bacterial genome are identified by using bidirectional BLASTP searches (best hits) and also based on synteny. The Clustal W package (http://ebi.ac.uk/clustalw) was used for polypeptide and nucleotide sequence alignments and phylogenetic footprinting analyses of promoters and Weblogo (http://weblogo.berkeley.edu) was applied to nucleotide sequence motif identification. The cellular localization of proteins in the cytoplasmic or periplasmic compartment was predicted using Signal P 4.1 server (http://cbs.dtu.dk/services/SignalP).
Genetic manipulation and genetic complementation
The two-step protocol of selection (gentamycin resistance (GmR) for single cross-over) and counter-selection (sucrose sensitivity for double crossover) was applied for in-frame deletion of specific genes using the suicide vector pDS3.0 (R6K replicon, sacB, GmR)-based constructs with a fusion of upstream and downstream sequences as previously described . The genes of S. oneidensis MR-1 was PCR amplified and cloned into the pHERD30T shuttle vector, which is suitable for cloning of toxic and tightly regulated genes like ECF sigma factor genes . The resultant constructs and empty vector were transferred into the MR-1 wild type strain and mutants as well as the P. aeruginosa PAO1 via conjugation.
RNA extraction, cDNA synthesis and RT-PCR analysis of gene transcription
Total RNA was extracted by using RNAiso Plus (Takara, Dalian, China) or RNAprep pure Cell/Bacteria Kit (Tiangen Biotech, Beijing, China) and RNA was further purified using DNase I treatment. The integrity of RNA was evaluated by agarose (0.8%) gel electrophoresis. The RNA concentration and purity was measured on a spectrophotometer (Nanodrop Technologies, Wilmington, DE, USA). To prepare cDNA, 2 μg of total RNA was reversely transcribed using PrimeScript® RT reagent Kit with gDNA Eraser (Takara, Dalian, China) and TIANscript RT Kit (TIANGEN BIOTECH (Beijing) CO., LTD.) according to the manufacturer’s protocol. The PCR thermal cycles were: 5 min at 95°C for cDNA denaturation, followed by 27–30 cycles of 30 s at 95°C, 30 s at 51-60°C and 30 s at 72°C. A final elongation step was performed for 10 min at 72°C. RT-PCR products were electrophoresed in a 0.8% agarose gel containing ethidium bromide and visualized by ultraviolet light and Bio-Rad Image software. The data presented are relative mRNA levels normalized against 16S rRNA transcript levels, and the value of the control was set to 1. All the experiments described were performed in triplicates or repeated three times in duplicates to obtain means and standard deviation (SD). The PCR products were also sequenced to confirm amplification of target genes. The primers used were listed in the supplemental materials (Additional file 1: Table S2).
Determination of transcription start site
Terminal deoxynucleotidyl transferase (TdT, Takara) was used to catalyze the incorporation of single deoxynucleotides (dATPs) into the 3′-OH terminus of cDNA to make the dA-tailed cDNA according to the producer’s protocol. Touchdown and nest PCR was used to amplify the dA-tailed cDNA by using an oligdT (5′-gccagtcTTTTTTTTTTTTTTTTT-3′) primer and a specific primer . The PCR product was cloned into pMD18-T vector (Takara, Dalian, China) for sequencing.
Hydrogen peroxide and paraquat sensitivity assay
To test the bacterial resistance to hydrogen peroxide (0, 0.1, 0.3, 0.5, 0.7 and 1 mM) and paraquat (0, 0.5, 1, 2, 3, and 4 mM) (1,1-dimethyl-4,4′-bipyridylium dichloride, a powerful propagator of superoxide radicals, Tokyo Chemical Industry Co., Tokyo, Japan) cells were grown overnight in LB broth containing different levels of each chemical and growth was monitored by measure optical density at 600 nm as previously described .
Expression, extraction and activity assays of hydrogen peroxidases
The glutathione hydrogen peroxidase (GPx) genes pgpD (lacking the N-terminal sequence encoding the signal peptide) and cgpD were cloned into the pET28a vector and the overproducing constructs were transferred into E. coli DE3/BL21 cells. The DE3 strains were grown in LB medium (supplemented with 100 μg/L of ampicillin) at 37°C to an OD600 of approximately 0.6 and the gene expression was induced by addition of IPTG (0.01%, w/v) at 16°C for 24 hours. The harvested E. coli cells were homogenized by applying high pressures (JN-02C low temperature ultra-high pressure continuous flow cell disrupter, Juneng Biol. & Technol. Co., Guangzhou, China) and the His-tagged recombinant proteins were purified by using Ni-NTA Sepharose (GE Healthcare, Waukesha, Wisconsin, USA) affinity chromatography according to the supplier’s protocol. The activity of hydrogen peroxidases is assayed by a widely used protocol with some modifications . 3 ml of the enzyme elute from Ni-NTA Sepharose was mixed with 3 ml of phosphate buffer containing 0.1 M hydrogen peroxide and 0.1 M glutathione (GSH). The reaction was stopped by adding 3 ml of 10% (v/v) sulfuric acid and the residual hydrogen peroxide was titrated against 0.1 M permanganate (KMnO4) solution until a faint purple color persisted for at least 30 seconds. The enzyme concentrations were measured by using a total protein assay kit (Jiancheng Biotech., Nanjing, China). The same amounts of boiling-denatured enzyme solutions were used as control.
Alkaline phosphatase A-fusion assay
To determine the protein cellular location, the 5′-nucleotide sequence, encoding the amino-terminal signal peptide (SP), of the pgpD gene was translationally fused with E. coli phoA gene with deletion of the sequence encoding the N-terminal signal sequence. This pgpD-phoA fusion and phoA were cloned into pUCP20T vector for alkaline phosphatase A-fusion assay , and the transformants of DH5α were plated on the LB plate containing 40 μg/ml of BCIP (5-Bromo-4-chloro-3-indolyl phosphate p-toluidine, Amresco, Solon, OH, USA) and 100 μg/ml of ampicillin. The construct pUCP20-phoA(wt) expressing full-length PhoA was used as positive control and the pUCP20-phoA(NSP) expressing the truncated PhoA without N-terminal signal leader sequence as negative control.
This work was supported by the Chinese Academy of Science Grant Y15103-1-401 and One-Hundred Scholar Award to D.Q. and the DOE grant DE-FG02-07ER64383 to J. Z.
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