1,506
Views
29
CrossRef citations to date
0
Altmetric
Research Papers

The sRNA SorY confers resistance during photooxidative stress by affecting a metabolite transporter in Rhodobacter sphaeroides

, &
Pages 569-577 | Received 05 Jan 2015, Accepted 13 Mar 2015, Published online: 06 May 2015

References

  • Dufour YS, Landick R, Donohue TJ. Organization and evolution of the biological response to singlet oxygen stress. J Mol Biol 2008; 383:713-30; PMID:18723027; http://dx.doi.org/10.1016/j.jmb.2008.08.017
  • Glaeser J, Nuss AM, Berghoff BA, Klug G. Singlet oxygen stress in microorganisms. Adv Microb Physiol 2011; 58:141-73; PMID:21722793; http://dx.doi.org/10.1016/B978-0-12-381043-4.00004-0
  • Braatsch S, Gomelsky M, Kuphal S, Klug G. A single flavoprotein, AppA, integrates both redox and light signals in Rhodobacter sphaeroides. Mol Microbiol 2002; 45:827-36; PMID:12139627; http://dx.doi.org/10.1046/j.1365-2958.2002.03058.x
  • Mank NN, Berghoff BA, Hermanns YN, Klug G. Regulation of bacterial photosynthesis genes by the small noncoding RNA PcrZ. Proc Natl Acad Sci U S A 2012; 109:16306-11; PMID:22988125; http://dx.doi.org/10.1073/pnas.1207067109
  • Han Y, Meyer MH, Keusgen M, Klug G. A haem cofactor is required for redox and light signalling by the AppA protein of Rhodobacter sphaeroides. Mol Microbiol 2007; 64:1090-104; PMID:17501930; http://dx.doi.org/10.1111/j.1365-2958.2007.05724.x
  • Anthony JR, Warczak KL, Donohue TJ. A transcriptional response to singlet oxygen, a toxic byproduct of photosynthesis. Proc Natl Acad Sci U S A 2005; 102:6502-7; PMID:15855269; http://dx.doi.org/10.1073/pnas.0502225102
  • Glaeser J, Klug G. Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes. Microbiology 2005; 151:1927-38; PMID:15942000; http://dx.doi.org/10.1099/mic.0.27789-0
  • Glaeser J, Zobawa M, Lottspeich F, Klug G. Protein synthesis patterns reveal a complex regulatory response to singlet oxygen in Rhodobacter. J Proteome Res 2007; 6:2460-71; PMID:17536848; http://dx.doi.org/10.1021/pr060624p
  • Berghoff BA, Glaeser J, Sharma CM, Vogel J, Klug G. Photooxidative stress-induced and abundant small RNAs in Rhodobacter sphaeroides. Mol Microbiol 2009; 74:1497-512; PMID:19906181; http://dx.doi.org/10.1111/j.1365-2958.2009.06949.x
  • Nuss AM, Glaeser J, Klug G. RpoH(II) activates oxidative-stress defense systems and is controlled by RpoE in the singlet oxygen-dependent response in Rhodobacter sphaeroides. J Bacteriol 2009; 191:220-30; PMID:18978062; http://dx.doi.org/10.1128/JB.00925-08
  • Anthony JR, Newman JD, Donohue TJ. Interactions between the Rhodobacter sphaeroides ECF sigma factor, sigma(E), and its anti-sigma factor, ChrR. J Mol Biol 2004; 341:345-60; PMID:15276828; http://dx.doi.org/10.1016/j.jmb.2004.06.018
  • Nuss AM, Adnan F, Weber L, Berghoff BA, Glaeser J, Klug G. DegS and RseP homologous proteases are involved in singlet oxygen dependent activation of RpoE in Rhodobacter sphaeroides. PLoS One 2013; 8:e79520; PMID:24223961; http://dx.doi.org/10.1371/journal.pone.0079520
  • Nam TW, Ziegelhoffer EC, Lemke RA, Donohue TJ. Proteins needed to activate a transcriptional response to the reactive oxygen species singlet oxygen. MBio 2013; 4:e00541-12; PMID:23300250; http://dx.doi.org/10.1128/mBio.00541-12
  • Karls RK, Brooks J, Rossmeissl P, Luedke J, Donohue TJ. Metabolic roles of a Rhodobacter sphaeroides member of the sigma32 family. J Bacteriol 1998; 180:10-9; PMID:9422586
  • Nuss AM, Glaeser J, Berghoff BA, Klug G. Overlapping alternative sigma factor regulons in the response to singlet oxygen in Rhodobacter sphaeroides. J Bacteriol 2010; 192:2613-23; PMID:20304993; http://dx.doi.org/10.1128/JB.01605-09
  • Berghoff BA, Glaeser J, Nuss AM, Zobawa M, Lottspeich F, Klug G. Anoxygenic photosynthesis and photooxidative stress: a particular challenge for Roseobacter. Environ Microbiol 2011; 13:775-91; PMID:21108722; http://dx.doi.org/10.1111/j.1462-2920.2010.02381.x
  • Berghoff BA, Konzer A, Mank NN, Looso M, Rische T, Forstner KU, Kruger M, Klug G. Integrative “omics”-approach discovers dynamic and regulatory features of bacterial stress responses. PLoS Genet 2013; 9:e1003576; PMID:23818867; http://dx.doi.org/10.1371/journal.pgen.1003576
  • Hess WR, Berghoff BA, Wilde A, Steglich C, Klug G. Riboregulators and the role of Hfq in photosynthetic bacteria. RNA Biol 2014; 11:413-26; PMID:24651049; http://dx.doi.org/10.4161/rna.28035
  • Waters LS, Storz G. Regulatory RNAs in bacteria. Cell 2009; 136:615-28; PMID:19239884; http://dx.doi.org/10.1016/j.cell.2009.01.043
  • Gottesman S. The small RNA regulators of Escherichia coli: roles and mechanisms*. Annu Rev Microbiol 2004; 58:303-28; PMID:15487940; http://dx.doi.org/10.1146/annurev.micro.58.030603.123841
  • Storz G, Altuvia S, Wassarman KM. An abundance of RNA regulators. Annu Rev Biochem 2005; 74:199-217; PMID:15952886; http://dx.doi.org/10.1146/annurev.biochem.74.082803.133136
  • Majdalani N, Vanderpool CK, Gottesman S. Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 2005; 40:93-113; PMID:15814430; http://dx.doi.org/10.1080/10409230590918702
  • Green HA, Donohue TJ. Activity of Rhodobacter sphaeroides RpoHII, a second member of the heat shock sigma factor family. J Bacteriol 2006; 188:5712-21; PMID:16885439; http://dx.doi.org/10.1128/JB.00405-06
  • Busch A, Richter AS, Backofen R. IntaRNA: efficient prediction of bacterial sRNA targets incorporating target site accessibility and seed regions. Bioinformatics 2008; 24:2849-56; PMID:18940824; http://dx.doi.org/10.1093/bioinformatics/btn544
  • Gonin S, Arnoux P, Pierru B, Lavergne J, Alonso B, Sabaty M, Pignol D. Crystal structures of an Extracytoplasmic Solute Receptor from a TRAP transporter in its open and closed forms reveal a helix-swapped dimer requiring a cation for alpha-keto acid binding. BMC Struct Biol 2007; 7:11; PMID:17362499; http://dx.doi.org/10.1186/1472-6807-7-11
  • Berghoff BA, Glaeser J, Sharma CM, Zobawa M, Lottspeich F, Vogel J, Klug G. Contribution of Hfq to photooxidative stress resistance and global regulation in Rhodobacter sphaeroides. Mol Microbiol 2011; 80:1479-95; PMID:21535243; http://dx.doi.org/10.1111/j.1365-2958.2011.07658.x
  • Thomas GH, Southworth T, Leon-Kempis MR, Leech A, Kelly DJ. Novel ligands for the extracellular solute receptors of two bacterial TRAP transporters. Microbiology 2006; 152:187-98; PMID:16385129; http://dx.doi.org/10.1099/mic.0.28334-0
  • Forward JA, Behrendt MC, Wyborn NR, Cross R, Kelly DJ. TRAP transporters: a new family of periplasmic solute transport systems encoded by the dctPQM genes of Rhodobacter capsulatus and by homologs in diverse gram-negative bacteria. J Bacteriol 1997; 179:5482-93; PMID:9287004
  • Shaw JG, Hamblin MJ, Kelly DJ. Purification, characterization and nucleotide sequence of the periplasmic C4-dicarboxylate-binding protein (DctP) from Rhodobacter capsulatus. Mol Microbiol 1991; 5:3055-62; PMID:1809844; http://dx.doi.org/10.1111/j.1365-2958.1991.tb01865.x
  • Braatsch S, Moskvin OV, Klug G, Gomelsky M. Responses of the Rhodobacter sphaeroides transcriptome to blue light under semiaerobic conditions. J Bacteriol 2004; 186:7726-35; PMID:15516587; http://dx.doi.org/10.1128/JB.186.22.7726-7735.2004
  • Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen J, Selbig J, Liu J, Fernie AR, Sweetlove LJ. The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol 2007; 143:312-25; PMID:17122072; http://dx.doi.org/10.1104/pp.106.090431
  • Rui B, Shen T, Zhou H, Liu J, Chen J, Pan X, Liu H, Wu J, Zheng H, Shi Y. A systematic investigation of Escherichia coli central carbon metabolism in response to superoxide stress. BMC Syst Biol 2010; 4:122; PMID:20809933; http://dx.doi.org/10.1186/1752-0509-4-122
  • Valdivia-Gonzalez M, Perez-Donoso JM, Vasquez CC. Effect of tellurite-mediated oxidative stress on the Escherichia coli glycolytic pathway. Biometals 2012; 25:451-8; PMID:22234496; http://dx.doi.org/10.1007/s10534-012-9518-x
  • Bignucolo A, Appanna VP, Thomas SC, Auger C, Han S, Omri A, Appanna VD. Hydrogen peroxide stress provokes a metabolic reprogramming in Pseudomonas fluorescens: enhanced production of pyruvate. J Biotechnol 2013; 167:309-15; PMID:23871654; http://dx.doi.org/10.1016/j.jbiotec.2013.07.002
  • Crimmins GT, Schelle MW, Herskovits AA, Ni PP, Kline BC, Meyer-Morse N, Iavarone AT, Portnoy DA. Listeria monocytogenes 6-Phosphogluconolactonase mutants induce increased activation of a host cytosolic surveillance pathway. Infect Immun 2009; 77:3014-22; PMID:19398547; http://dx.doi.org/10.1128/IAI.01511-08
  • Blanchard JL, Wholey WY, Conlon EM, Pomposiello PJ. Rapid changes in gene expression dynamics in response to superoxide reveal SoxRS-dependent and independent transcriptional networks. PLoS One 2007; 2:e1186; http://dx.doi.org/10.1371/journal.pone.0001186
  • Rungrassamee W, Liu X, Pomposiello PJ. Activation of glucose transport under oxidative stress in Escherichia coli. Arch Microbiol 2008; 190:41-9; PMID:18368388; http://dx.doi.org/10.1007/s00203-008-0361-y
  • Singh R, Lemire J, Mailloux RJ, Appanna VD. A novel strategy involved in anti-oxidative defense: the conversion of NADH into NADPH by a metabolic network. PLoS One 2008; 3:e2682; PMID:18628998; http://dx.doi.org/10.1371/journal.pone.0002682
  • Imam S, Noguera DR, Donohue TJ. Global insights into energetic and metabolic networks in Rhodobacter sphaeroides. BMC Syst Biol 2013; 7:89; PMID:24034347; http://dx.doi.org/10.1186/1752-0509-7-89
  • Dufour YS, Imam S, Koo BM, Green HA, Donohue TJ. Convergence of the transcriptional responses to heat shock and singlet oxygen stresses. PLoS Genet 2012; 8:e1002929; PMID:23028346; http://dx.doi.org/10.1371/journal.pgen.1002929
  • Altuvia S, Weinstein-Fischer D, Zhang A, Postow L, Storz G. A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 1997; 90:43-53; PMID:9230301; http://dx.doi.org/10.1016/S0092-8674(00)80312-8
  • Gonzalez-Flecha B, Demple B. Role for the oxyS gene in regulation of intracellular hydrogen peroxide in Escherichia coli. J Bacteriol 1999; 181:3833-6; PMID:10368161
  • Masse E, Gottesman S. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci U S A 2002; 99:4620-5; PMID:11917098; http://dx.doi.org/10.1073/pnas.032066599
  • Wilderman PJ, Sowa NA, FitzGerald DJ, FitzGerald PC, Gottesman S, Ochsner UA, Vasil ML. Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc Natl Acad Sci U S A 2004; 101:9792-7; PMID:15210934; http://dx.doi.org/10.1073/pnas.0403423101
  • Boughammoura A, Matzanke BF, Bottger L, Reverchon S, Lesuisse E, Expert D, Franza T. Differential role of ferritins in iron metabolism and virulence of the plant-pathogenic bacterium Erwinia chrysanthemi 3937. J Bacteriol 2008; 190:1518-30; PMID:18165304; http://dx.doi.org/10.1128/JB.01640-07
  • Touati D. Iron and oxidative stress in bacteria. Arch Biochem Biophys 2000; 373:1-6; PMID:10620317; http://dx.doi.org/10.1006/abbi.1999.1518
  • Varghese S, Tang Y, Imlay JA. Contrasting sensitivities of Escherichia coli aconitases A and B to oxidation and iron depletion. J Bacteriol 2003; 185:221-30; PMID:12486059; http://dx.doi.org/10.1128/JB.185.1.221-230.2003
  • Vogel J, Papenfort K. Small non-coding RNAs and the bacterial outer membrane. Curr Opin Microbiol 2006; 9:605-11; PMID:17055775; http://dx.doi.org/10.1016/j.mib.2006.10.006
  • Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, Vogel J. Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 2009; 74:139-58; PMID:19732340; http://dx.doi.org/10.1111/j.1365-2958.2009.06857.x
  • Remes B, Berghoff BA, Forstner KU, Klug G. Role of oxygen and the OxyR protein in the response to iron limitation in Rhodobacter sphaeroides. BMC Genomics 2014; 15:794; PMID:25220182; http://dx.doi.org/10.1186/1471-2164-15-794
  • Glaeser J, Klug G. Photo-oxidative stress in Rhodobacter sphaeroides: Protective role of carotenoids and expression of selected genes. Microbiology 2005; 151:1927-38; PMID:15942000; http://dx.doi.org/10.1099/mic.0.27789-0
  • Janzon L, Löfdahl S, Arvidson S. Evidence for a coordinate transcriptional control of alpha-toxin and protein a synthesis in Staphylococcus aureus. FEMS Microbiol Lett 1986; 33:193-8; http://dx.doi.org/10.1111/j.1574-6968.1986.tb01270.x
  • Zeller T, Klug G. Detoxification of hydrogen peroxide and expression of catalase genes in Rhodobacter. Microbiology 2004; 150:3451-62; PMID:15470122; http://dx.doi.org/10.1099/mic.0.27308-0
  • Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29:e45; PMID:11328886; http://dx.doi.org/10.1093/nar/29.9.e45
  • Church GM, Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A 1984; 81:1991-5; PMID:6326095; http://dx.doi.org/10.1073/pnas.81.7.1991