2,387
Views
10
CrossRef citations to date
0
Altmetric
Research Article

RpoS-regulated SEN1538 gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence

, , , & ORCID Icon

References

  • Fang FC, Frawley ER, Tapscott T, et al. Bacterial Stress Responses during Host Infection. Cell Host Microbe. 2016;20:133–143.
  • Shu S, Ferric CF. Integrated stress response in Salmonella. Int J Food Microbiol. 2012;152:75–81.
  • Fàbrega A, Vila J. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev. 2013;26:308–341.
  • Balasubramanian R, Im J, Lee J-S, et al. The global burden and epidemiology of invasive non-typhoidal Salmonella infections. Hum Vaccin Immunother. 2018;00:1–6.
  • Betancor L, Yim L, Fookes M, et al. Genomic and phenotypic variation in epidemic-spanning Salmonella enterica serovar Enteritidis isolates. BMC Microbiol. 2009;9:1–16.
  • Bader MW, Navarre WW, Shiau W, et al. Regulation of Salmonella Typhimurium virulence gene expression by cationic antimicrobial peptides. Mol Microbiol. 2003;50:219–230.
  • Doyle ME, Mazzotta AS. Review of studies on the thermal resistance of Salmonellae. J Food Prot. 2000;63:779–795.
  • Spector MP, Del Portillo FG, Bearson SMD, et al. The rpoS-dependent starvation-stress response locus stiA encodes a nitrate reductase (narZYWV) required for carbon-starvation-inducible thermotolerance and acid tolerance in Salmonella typhimurium. Microbiology. 1999;145:3035–3045.
  • Ebrahimi A, Csonka LN, Alam MA. Analyzing thermal stability of cell membrane of Salmonella using time-multiplexed impedance sensing. Biophys J. 2018;114:609–618.
  • Sirsat SA, Burkholder KM, Muthaiyan A, et al. Effect of sublethal heat stress on Salmonella typhimurium virulence. J Appl Microbiol. 2011;110:813–822.
  • Rychlik I, Barrow PA. Salmonella stress management and its relevance to behaviour during intestinal colonisation and infection. FEMS Microbiol Rev. 2005;29:1021–1040.
  • Alhenaky A, Abdelqader A, Abuajamieh M, et al. The effect of heat stress on intestinal integrity and Salmonella invasion in broiler birds. J Therm Biol. 2017;70:9–14.
  • Battesti A, Majdalani N, Gottesman S. The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol. 2011;65:189–213.
  • Lago M, Monteil V, Douche T, et al. Proteome remodelling by the stress sigma factor RpoS/σS in Salmonella: identification of small proteins and evidence for post-transcriptional regulation. Sci Rep. 2017;7:1–15.
  • Weber H, Polen T, Heuveling J, et al. Genome-wide analysis of the general stress response network in Escherichia coli: sigma S-dependent genes, promoters, and sigma factor selectivity†. J Bacteriol. 2005;187:1591–1603.
  • Ibanez-Ruiz M, Robbe-Saule V, Hermant D, et al. Identification of RpoS (sigma(S))-regulated genes in Salmonella enterica serovar typhimurium. J Bacteriol. 2000;182:5749–5756.
  • Robbe-Saule V, Lopes MD, Kolb A, et al. Physiological effects of crl in Salmonella are modulated by σS level and promoter specificity. J Bacteriol. 2007;189:2976–2987.
  • Vijayakumar SRV, Kirchhof MG, Patten CL, et al. RpoS-regulated genes of Escherichia coli Identified by random lacZ fusion mutagenesis. J Bacteriol. 2004;186:8499–8507.
  • Oguri T, Kwon Y, Woo JKK, et al. A family of small intrinsically disordered proteins involved in flagellum-dependent motility in Salmonella enterica. J Bacteriol. 2019;201:1–18.
  • Ryan D, Pati NB, Ojha UK, et al. Global transcriptome and mutagenic analyses of the acid tolerance response of Salmonella enterica serovar typhimurium. Appl Environ Microbiol. 2015;81:8054–8065.
  • Robbe-Saule V, Coynault C, Ibanez-Ruiz M, et al. Identification of a non-haem catalase in Salmonella and its regulation by RpoS (σS). Mol Microbiol. 2001;39:1533–1545.
  • Barthel M, Hapfelmeier S, Quintanilla-Martínez L, et al. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun. 2003;71:2839–2858.
  • Vishwakarma V, Periaswamy B, Bhusan Pati N, et al. A novel phage element of Salmonella enterica serovar enteritidis P125109 contributes to accelerated Type III secretion system 2-dependent early inflammation kinetics in a mouse colitis model. Infect Immun. 2012;80:3236–3246.
  • Pilonieta MC, Nagy TA, Jorgensen DR, et al. A glycine betaine importer limits Salmonella stress resistance and tissue colonization by reducing trehalose production. Mol Microbiol. 2012;84:296–309.
  • Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci. 2000;97:6640–6645.
  • Uzzau S, Figueroa-Bossi N, Rubino S, et al. Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A. 2001;98:15264–15269.
  • Moreira CG, Herrera CM, Needham BD, et al. Virulence and stress-related periplasmic protein (VisP) in bacterial/host associations. Proc Natl Acad Sci. 2013;110:1470–1475.
  • Hernández SB, Cota I, Ducret A, et al. Adaptation and preadaptation of Salmonella enterica to Bile. PLoS Genet. 2012;8:1–15.
  • Das S, Ray S, Ryan D, et al. Identification of a novel gene in ROD9 island of Salmonella Enteritidis involved in the alteration of virulence-associated genes expression. Virulence. 2018;9:348–362.
  • Das JK, Mishra D, Ray P, et al. In vitro evaluation of anti-infective activity of a Lactobacillus plantarum strain against Salmonella enterica serovar Enteritidis. Gut Pathog. 2013;5:11.
  • Suar M, Periaswamy B, Songhet P, et al. Accelerated Type III secretion system 2-dependent enteropathogenesis by a Salmonella enterica serovar enteritidis PT4/6 strain. Infect Immun. 2009;77:3569–3577.
  • Patel RK, Jain M. NGS QC toolkit: a toolkit for quality control of next generation sequencing data. PLoS One. 2012;7:e30619.
  • McClure R, Balasubramanian D, Sun Y, et al. Computational analysis of bacterial RNA-Seq data. Nucleic Acids Res. 2013;41:1–16.
  • GarcíaVéscov E, Soncini FC, Groisman EA. Mg2+ as an extracellular signal: environmental regulation of Salmonella Virulence. Cell. 1996;84:165–174.
  • Groisman EA, Hollands K, Kriner MA, et al. Bacterial Mg2+ homeostasis, transport, and virulence. Annu Rev Genet. 2013;47:625–646.
  • Groisman EA, Kayser J, Soncini FC. Regulation of polymyxin resistance and adaptation to Low-Mg2+ environments. J Bacteriol. 1997;179:7040–7045.
  • Martynowycz MW, Rice A, Andreev K, et al. Salmonella membrane structural remodeling increases resistance to antimicrobial peptide LL-37. ACS Infect Dis. 2019;5:1214–1222.
  • Pin C, Hansen T, Oz-Cuevas MM, et al. The transcriptional heat shock response of Salmonella typhimurium shows hysteresis and heated cells show increased resistance to heat and acid stress. PLoS One. 2012;7:1–10.
  • Beraud M, Kolb A, Monteil V, et al. A proteomic analysis reveals differential regulation of the σS-dependent yciGFE(katN) locus by YncC and H-NS in Salmonella and Escherichia coli K-12. Mol Cell Proteomics. 2010;9:2601–2616.
  • Papp-wallace KM, Nartea M, Kehres DG, et al. The CorA Mg2+ channel is required for the virulence of Salmonella enterica serovar typhimurium. J Bacteriol. 2008;190:6517–6523.
  • Spector MP, Kenyon WJ. Resistance and survival strategies of Salmonella enterica to environmental stresses. Food Res Int. 2012;45:455–481.
  • Fang FC, Libby SJ, Buchmeier NA, et al. The alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc Natl Acad Sci. 1992;89:11978–11982.
  • Lévi-Meyrueis C, Monteil V, Sismeiro O, et al. Expanding the RpoS/σS-network by RNA sequencing and identification of σS-controlled small RNAs in Salmonella. PLoS One. 2014;9:1–12.
  • Lelong C, Aguiluz K, Luche S, et al. The Crl-RpoS regulon of Escherichia coli. Mol Cell Proteomics. 2007;6:648–659.
  • Hengge-Aronis R. Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev. 2002;66:373–395.
  • Dong T, Schellhorn HE. Control of RpoS in global gene expression of Escherichia coli in minimal media. Mol Genet Genomics. 2009;281:19–33.
  • Patten CL, Kirchhof MG, Schertzberg MR, et al. Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Genet Genomics. 2004;272:580–591.
  • Chen CYI, Eckmann L, Libby SJ, et al. Expression of Salmonella typhimurium rpoS and rpoS-dependent genes in the intracellular environment of eukaryotic cells. Infect Immun. 1996;64:4739–4743.
  • Tamayo R, Ryan SS, Mccoy AJ, et al. Identification and Genetic Characterization of PmrA-Regulated Genes and Genes Involved in Polymyxin B Resistance in Salmonella enterica Serovar Typhimurium. Infect Immun. 2002;70:6770–6778.
  • Connor KO, Fletcher SA, Csonka LN. Increased expression of Mg2+ transport proteins enhances the survival of Salmonella enterica at high temperature. Proc Natl Acad Sci. 2009;106:17522–17527.
  • Ray S, Costa R, Das M, et al. Interplay of cold shock protein E with an uncharacterized protein, YciF, lowers porin expression and enhances bile resistance in Salmonella typhimurium. J Biol Chem. 2019;294:9084–9099.
  • Prouty AM, Brodsky IE, Manos J, et al. Transcriptional regulation of Salmonella enterica serovar typhimurium genes by bile. FEMS Immunol Med Microbiol. 2004;41:177–185.
  • Xia X, Zhang L, Wang Y. The antimicrobial peptide cathelicidin-BF could be a potential therapeutic for Salmonella typhimurium infection. Microbiol Res. 2015;171:45–51.
  • Lewis C, Skovierova H, Rowley G, et al. Salmonella enterica Serovar Typhimurium HtrA : regulation of expression and role of the chaperone and protease activities during infection. Microbiology. 2019;155:873–881.
  • Groisman EA, Parra-Lopez C, Salcedo M, et al. Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc Natl Acad Sci. 2006;89:11939–11943.
  • Eswarappa SM, Panguluri KK, Hensel M, et al. The yejABEF operon of Salmonella confers resistance to antimicrobial peptides and contributes to its virulence. Microbiology. 2008;154:666–678.
  • Gunn JS, Ryan SS, Van Velkinburgh JC, et al. Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar typhimurium. Infect Immun. 2002;68:6139–6146.
  • Herrou J, Willett JW, Czyz DM, et al. Conserved ABC transport system regulated by the general stress response pathways of alpha- and gammaproteobacteria. J Bacteriol. 2017;199:1–18.
  • Felgner S, Frahm M, Kocijancic D, et al. aroA -deficient Salmonella enterica serovar typhimurium is more than a metabolically attenuated mutant. MBio. 2016;7:1–12.
  • Oldfield CJ, Dunker AK. Intrinsically disordered proteins and intrinsically disordered protein regions. Annu Rev Biochem. 2014;83:553–584.