A comparative proteomic analysis of Salmonella typhimurium under the regulation of the RstA/RstB and PhoP/PhoQ systems

Tran, Trung; Han, Qiang Qiang; Shi, Yixin; Guo, Lin

doi:10.1016/j.bbapap.2016.09.003

Cited by 23 publications

(21 citation statements)

References 48 publications

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“…The RstAB regulon seems to be little predictive: whereas E. coli RstAB positively regulates the three genes yfiA , entE and cspC (Oshima et al, 2002), expression of yfiA and cspC in S. enterica remained unaffected both under over-expression of rstA and under deletion of rstA (Cabeza et al, 2007). A recent study evidenced that a S. enterica rstB mutant had reduced expression levels of genes related to pyrimidine metabolism ( udp and cdd genes), enterobactin biosynthesis ( entA , entB , entE , and entF ) and ferrous iron transport ( feoA , feoB ) (Tran et al, 2016). These results thus suggest that the RstAB TCS of different species, although phylogenetically closely-related, govern the expression of distinct groups of genes in different bacteria.…”

Section: Discussionmentioning

confidence: 99%

rstB Regulates Expression of the Photobacterium damselae subsp. damselae Major Virulence Factors Damselysin, Phobalysin P and Phobalysin C

et al. 2017

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The marine pathogenic bacterium Photobacterium damselae subsp. damselae causes septicemia in marine animals and in humans. The pPHDD1 plasmid-encoded hemolysins damselysin (Dly) and phobalysin P (PhlyP), and the chromosome-encoded hemolysin phobalysin C (PhlyC) constitute its main virulence factors. However, the mechanisms by which expression of these three hemolysins is regulated remain unknown. Here we report the isolation of a mini-Tn10 transposon mutant which showed a strong impairment in its hemolytic activity. The transposon disrupted a putative sensor histidine kinase gene vda_000600 (rstB), which together with vda_000601 (rstA) is predicted to encode a putative two-component regulatory system. This system showed to be homologous to the Vibrio cholerae CarSR/VprAB and Escherichia coli RstAB systems. Reconstruction of the mutant by allelic exchange of rstB showed equal impairment in hemolysis, and complementation with a plasmid expressing rstAB restored hemolysis to wild-type levels. Remarkably, we demonstrated by promoter expression analyses that the reduced hemolysis in the rstB mutant was accompanied by a strong decrease in transcription activities of the three hemolysin genes dly (damselysin), hlyApl (phobalysin P) and hlyAch (phobalysin C). Thus, RstB, encoded in the small chromosome, regulates plasmid and chromosomal virulence genes. We also found that reduced expression of the three virulence genes correlated with a strong decrease in virulence in a sea bass model, demonstrating that RstB constitutes a master regulator of the three P. damselae subsp. damselae hemolysins and plays critical roles in the pathogenicity of this bacterium. This study represents the first evidence of a direct role of a RstAB-like system in the regulation of bacterial toxins.

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Section: Discussionmentioning

confidence: 99%

rstB Regulates Expression of the Photobacterium damselae subsp. damselae Major Virulence Factors Damselysin, Phobalysin P and Phobalysin C

et al. 2017

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“…In addition, the proteins should contain at least one identified peptide. The false discovery rates (FDR) for identification of proteins and peptides using decoy method by Scaffold software should to be less than or equal to 1% (FDR ≤ 1%) [ 54 , 58 , 59 ]. For the protein quantitation, the quantitative value of total ion current (TIC) of each protein was normalized by sum total of TIC.…”

Section: Methodsmentioning

confidence: 99%

N-dodecanoyl-homoserine lactone influences the levels of thiol and proteins related to oxidation-reduction process in Salmonella

et al. 2018

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Quorum sensing is a cell-cell communication mechanism mediated by chemical signals that leads to differential gene expression in response to high population density. Salmonella is unable to synthesize the autoinducer-1 (AI-1), N-acyl homoserine lactone (AHL), but is able to recognize AHLs produced by other microorganisms through SdiA protein. This study aimed to evaluate the fatty acid and protein profiles of Salmonella enterica serovar Enteritidis PT4 578 throughout time of cultivation in the presence of AHL. The presence of N-dodecanoyl-homoserine lactone (C12-HSL) altered the fatty acid and protein profiles of Salmonella cultivated during 4, 6, 7, 12 and 36 h in anaerobic condition. The profiles of Salmonella Enteritidis at logarithmic phase of growth (4 h of cultivation), in the presence of C12-HSL, were similar to those of cells at late stationary phase (36 h). In addition, there was less variation in both protein and fatty acid profiles along growth, suggesting that this quorum sensing signal anticipated a stationary phase response. The presence of C12-HSL increased the abundance of thiol related proteins such as Tpx, Q7CR42, Q8ZP25, YfgD, AhpC, NfsB, YdhD and TrxA, as well as the levels of free cellular thiol after 6 h of cultivation, suggesting that these cells have greater potential to resist oxidative stress. Additionally, the LuxS protein which synthesizes the AI-2 signaling molecule was differentially abundant in the presence of C12-HSL. The NfsB protein had its abundance increased in the presence of C12-HSL at all evaluated times, which is a suggestion that the cells may be susceptible to the action of nitrofurans or that AHLs present some toxicity. Overall, the presence of C12-HSL altered important pathways related to oxidative stress and stationary phase response in Salmonella.

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“…Most importantly, in many pathogens PhoP/PhoR TCSs have also been shown to regulate pathogenesis (Perez et al, 2001; Ryndak et al, 2008). PhoP and PhoQ TCS components have been reported in many Gram-negative bacteria, including E. coli (Eguchi et al, 2007), Edwardsvilla (Lv et al, 2012), and Salmonella (Tran et al, 2016). PhoP/PhoR is also an important TCS in M. tuberculosis and is a key player in virulence (Ryndak et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

“…In particular, PhoP/PhoQ TCSs control the transcription of key virulent genes in several bacterial pathogens, including Escherichia coli, Shigella spp. (Tobe, 2008), Yersinia pestis (O'Loughlin et al, 2010), and Salmonella typhimurium (Tran et al, 2016). TCSs also control the expression of Pneumococcal surface antigen A (PsaA), subsequently regulating virulence and resistance to oxidative stress in Streptococcus pneumonia (McCluskey et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

A Novel RAYM_RS09735/RAYM_RS09740 Two-Component Signaling System Regulates Gene Expression and Virulence in Riemerella anatipestifer

Wang

Yin

et al. 2017

Front. Microbiol.

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The Gram-negative bacterium Riemerella anatipestifer is an important waterfowl pathogen, causing major economic losses to the duck-producing industry. However, little is known of the virulence factors that mediate pathogenesis during R. anatipestifer infection. In this study, RAYM_RS09735 and RAYM_RS09740 were predicted to form a two-component signaling system (TCS) through bioinformatics analysis. This TCS was highly conserved across the Flavobacteriaceae. A mutant YMΔRS09735/RS09740 strain was constructed to investigate the role of the RAYM_RS09735/RAYM_RS09740 TCS in R. anatipestifer virulence and gene regulation. The median lethal dose (LD50) of YMΔRS09735/RS09740 was found to be >1011 CFU, equivalent to that of avirulent bacterial strains. The bacterial abundances of the YMΔRS09735/RS09740 strain in the heart, brain, liver, blood, and spleen were significantly lower than that of the wild-type R. anatipestifer YM strain. Pathological analysis using hematoxylin and eosin staining showed that, compared to the wild-type, the mutant YMΔRS09735/RS09740 strain caused significantly less virulence in infected ducklings. RNAseq and real-time PCR analysis indicated that the RAYM_RS09735/RAYM_RS09740 TCS is a PhoP/PhoR system. This is a novel type of TCS for Gram-negative bacteria. The TCS was also found to be a global regulator of expression in R. anatipestifer, with 112 genes up-regulated and 693 genes down-regulated in the YMΔRS09735/RS09740 strain (~33% genes demonstrated differential expression). In summary, we have reported the first PhoP/PhoR TCS identified in a Gram-negative bacterium and demonstrated that it is involved in virulence and gene regulation in R. anatipestifer.

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A comparative proteomic analysis of Salmonella typhimurium under the regulation of the RstA/RstB and PhoP/PhoQ systems

Cited by 23 publications

References 48 publications

rstB Regulates Expression of the Photobacterium damselae subsp. damselae Major Virulence Factors Damselysin, Phobalysin P and Phobalysin C

rstB Regulates Expression of the Photobacterium damselae subsp. damselae Major Virulence Factors Damselysin, Phobalysin P and Phobalysin C

N-dodecanoyl-homoserine lactone influences the levels of thiol and proteins related to oxidation-reduction process in Salmonella

A Novel RAYM_RS09735/RAYM_RS09740 Two-Component Signaling System Regulates Gene Expression and Virulence in Riemerella anatipestifer

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