The alarmones (p)ppGpp are part of the heat shock response of Bacillus subtilis

. 2020 Mar ; 16 (3) : e1008275. [epub] 20200316

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32176689
Odkazy

PubMed 32176689
PubMed Central PMC7098656
DOI 10.1371/journal.pgen.1008275
PII: PGENETICS-D-19-01023
Knihovny.cz E-zdroje

Bacillus subtilis cells are well suited to study how bacteria sense and adapt to proteotoxic stress such as heat, since temperature fluctuations are a major challenge to soil-dwelling bacteria. Here, we show that the alarmones (p)ppGpp, well known second messengers of nutrient starvation, are also involved in the heat stress response as well as the development of thermo-resistance. Upon heat-shock, intracellular levels of (p)ppGpp rise in a rapid but transient manner. The heat-induced (p)ppGpp is primarily produced by the ribosome-associated alarmone synthetase Rel, while the small alarmone synthetases RelP and RelQ seem not to be involved. Furthermore, our study shows that the generated (p)ppGpp pulse primarily acts at the level of translation, and only specific genes are regulated at the transcriptional level. These include the down-regulation of some translation-related genes and the up-regulation of hpf, encoding the ribosome-protecting hibernation-promoting factor. In addition, the alarmones appear to interact with the activity of the stress transcription factor Spx during heat stress. Taken together, our study suggests that (p)ppGpp modulates the translational capacity at elevated temperatures and thereby allows B. subtilis cells to respond to proteotoxic stress, not only by raising the cellular repair capacity, but also by decreasing translation to concurrently reduce the protein load on the cellular protein quality control system.

Zobrazit více v PubMed

Storz G, Hengge R, American Society for Microbiology, editors. Bacterial stress responses. 2nd ed Washington, DC: ASM Press; 2011.

Mogk A, Huber D, Bukau B. Integrating protein homeostasis strategies in prokaryotes. Cold Spring Harb Perspect Biol. 2011;3 10.1101/cshperspect.a004366 PubMed DOI PMC

Hartl FU, Bracher A, Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature. 2011;475: 324–332. 10.1038/nature10317 PubMed DOI

Lindquist S. The Heat-Shock Response. Annual Review of Biochemistry. 1986;55: 1151–1191. 10.1146/annurev.bi.55.070186.005443 PubMed DOI

Lim B, Gross CA. Cellular Response to Heat Shock and Cold Shock In: Storz G, Hengge R, editors. Bacterial stress responses 2nd edition Washington, DC: ASM press, American Society for Microbiology; 2010. pp. 93–114.

Helmann JD, Wu MF, Kobel PA, Gamo FJ, Wilson M, Morshedi MM, et al. Global transcriptional response of Bacillus subtilis to heat shock. J Bacteriol. 2001;183: 7318–7328. 10.1128/JB.183.24.7318-7328.2001 PubMed DOI PMC

Winkler J, Seybert A, Konig L, Pruggnaller S, Haselmann U, Sourjik V, et al. Quantitative and spatio-temporal features of protein aggregation in Escherichia coli and consequences on protein quality control and cellular ageing. EMBO J. 2010;29: 910–23. 10.1038/emboj.2009.412 PubMed DOI PMC

Völker U, Mach H, Schmid R, Hecker M. Stress proteins and cross-protection by heat shock and salt stress in Bacillus subtilis. J Gen Microbiol. 1992;138: 2125–2135. 10.1099/00221287-138-10-2125 PubMed DOI

Runde S, Molière N, Heinz A, Maisonneuve E, Janczikowski A, Elsholz AKW, et al. The role of thiol oxidative stress response in heat-induced protein aggregate formation during thermotolerance in B acillus subtilis: Thiol oxidation in protein aggregate formation. Molecular Microbiology. 2014;91: 1036–1052. PubMed

Hecker M, Schumann W, Völker U. Heat-shock and general stress response in Bacillus subtilis. Molecular microbiology. 1996;19: 417–428. 10.1046/j.1365-2958.1996.396932.x PubMed DOI

Mogk A, Homuth G, Scholz C, Kim L, Schmid FX, Schumann W. The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. EMBO J. 1997;16: 4579–4590. 10.1093/emboj/16.15.4579 PubMed DOI PMC

Krüger E, Hecker M. The first gene of the Bacillus subtilis clpC operon, ctsR, encodes a negative regulator of its own operon and other class III heat shock genes. J Bacteriol. 1998;180: 6681–6688. PubMed PMC

Elsholz AKW, Michalik S, Zühlke D, Hecker M, Gerth U. CtsR, the Gram-positive master regulator of protein quality control, feels the heat. The EMBO Journal. 2010;29: 3621–3629. 10.1038/emboj.2010.228 PubMed DOI PMC

Hecker M, Pané-Farré J, Völker U. SigB-Dependent General Stress Response in Bacillus subtilis and Related Gram-Positive Bacteria. Annual Review of Microbiology. 2007;61: 215–236. 10.1146/annurev.micro.61.080706.093445 PubMed DOI

Nakano S, Küster-Schöck E, Grossman AD, Zuber P. Spx-dependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis. Proc Natl Acad Sci USA. 2003;100: 13603–13608. 10.1073/pnas.2235180100 PubMed DOI PMC

Rochat T, Nicolas P, Delumeau O, Rabatinová A, Korelusová J, Leduc A, et al. Genome-wide identification of genes directly regulated by the pleiotropic transcription factor Spx in Bacillus subtilis. Nucleic Acids Res. 2012;40: 9571–9583. 10.1093/nar/gks755 PubMed DOI PMC

Schäfer H, Heinz A, Sudzinová P, Voß M, Hantke I, Krásný L, et al. Spx, the central regulator of the heat and oxidative stress response in B. subtilis, can repress transcription of translation-related genes. Mol Microbiol. 2019;111: 514–533. 10.1111/mmi.14171 PubMed DOI

Leichert LIO, Scharf C, Hecker M. Global characterization of disulfide stress in Bacillus subtilis. J Bacteriol. 2003;185: 1967–1975. 10.1128/JB.185.6.1967-1975.2003 PubMed DOI PMC

Potrykus K, Cashel M. (p)ppGpp: still magical? Annu Rev Microbiol. 2008;62: 35–51. 10.1146/annurev.micro.62.081307.162903 PubMed DOI

Hauryliuk V, Atkinson GC, Murakami KS, Tenson T, Gerdes K. Recent functional insights into the role of (p)ppGpp in bacterial physiology. Nat Rev Microbiol. 2015;13: 298–309. 10.1038/nrmicro3448 PubMed DOI PMC

Haseltine WA, Block R. Synthesis of guanosine tetra- and pentaphosphate requires the presence of a codon-specific, uncharged transfer ribonucleic acid in the acceptor site of ribosomes. Proc Natl Acad Sci USA. 1973;70: 1564–1568. 10.1073/pnas.70.5.1564 PubMed DOI PMC

Wendrich TM, Blaha G, Wilson DN, Marahiel MA, Nierhaus KH. Dissection of the Mechanism for the Stringent Factor RelA. Molecular Cell. 2002;10: 779–788. 10.1016/s1097-2765(02)00656-1 PubMed DOI

Arenz S, Abdelshahid M, Sohmen D, Payoe R, Starosta AL, Berninghausen O, et al. The stringent factor RelA adopts an open conformation on the ribosome to stimulate ppGpp synthesis. Nucleic Acids Res. 2016;44: 6471–6481. 10.1093/nar/gkw470 PubMed DOI PMC

Brown A, Fernández IS, Gordiyenko Y, Ramakrishnan V. Ribosome-dependent activation of stringent control. Nature. 2016;534: 277–280. 10.1038/nature17675 PubMed DOI PMC

Loveland AB, Bah E, Madireddy R, Zhang Y, Brilot AF, Grigorieff N, et al. Ribosome•RelA structures reveal the mechanism of stringent response activation. Elife. 2016;5 10.7554/eLife.17029 PubMed DOI PMC

Atkinson GC, Tenson T, Hauryliuk V. The RelA/SpoT Homolog (RSH) Superfamily: Distribution and Functional Evolution of ppGpp Synthetases and Hydrolases across the Tree of Life. Stiller JW, editor. PLoS ONE. 2011;6: e23479 10.1371/journal.pone.0023479 PubMed DOI PMC

Wendrich TM, Marahiel MA. Cloning and characterization of a relA/spoT homologue from Bacillus subtilis. Mol Microbiol. 1997;26: 65–79. 10.1046/j.1365-2958.1997.5511919.x PubMed DOI

Nanamiya H, Kasai K, Nozawa A, Yun C-S, Narisawa T, Murakami K, et al. Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis. Mol Microbiol. 2008;67: 291–304. 10.1111/j.1365-2958.2007.06018.x PubMed DOI

Srivatsan A, Han Y, Peng J, Tehranchi AK, Gibbs R, Wang JD, et al. High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet. 2008;4: e1000139 10.1371/journal.pgen.1000139 PubMed DOI PMC

Boutte CC, Crosson S. Bacterial lifestyle shapes stringent response activation. Trends Microbiol. 2013;21: 174–180. 10.1016/j.tim.2013.01.002 PubMed DOI PMC

Irving SE, Corrigan RM. Triggering the stringent response: signals responsible for activating (p)ppGpp synthesis in bacteria. Microbiology. 2018;164: 268–276. 10.1099/mic.0.000621 PubMed DOI

Lopez JM, Dromerick A, Freese E. Response of guanosine 5’-triphosphate concentration to nutritional changes and its significance for Bacillus subtilis sporulation. J Bacteriol. 1981;146: 605–613. PubMed PMC

Kriel A, Bittner AN, Kim SH, Liu K, Tehranchi AK, Zou WY, et al. Direct regulation of GTP homeostasis by (p)ppGpp: a critical component of viability and stress resistance. Mol Cell. 2012;48: 231–241. 10.1016/j.molcel.2012.08.009 PubMed DOI PMC

Krásný L, Gourse RL. An alternative strategy for bacterial ribosome synthesis: Bacillus subtilis rRNA transcription regulation. EMBO J. 2004;23: 4473–4483. 10.1038/sj.emboj.7600423 PubMed DOI PMC

Krásný L, Tišerová H, Jonák J, Rejman D, Šanderová H. The identity of the transcription +1 position is crucial for changes in gene expression in response to amino acid starvation in Bacillus subtilis. Molecular Microbiology. 2008;69: 42–54. 10.1111/j.1365-2958.2008.06256.x PubMed DOI

Geiger T, Wolz C. Intersection of the stringent response and the CodY regulon in low GC Gram-positive bacteria. Int J Med Microbiol. 2014;304: 150–155. 10.1016/j.ijmm.2013.11.013 PubMed DOI

Ratnayake-Lecamwasam M, Serror P, Wong KW, Sonenshein AL. Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev. 2001;15: 1093–1103. 10.1101/gad.874201 PubMed DOI PMC

Milon P, Tischenko E, Tomsic J, Caserta E, Folkers G, La Teana A, et al. The nucleotide-binding site of bacterial translation initiation factor 2 (IF2) as a metabolic sensor. Proc Natl Acad Sci USA. 2006;103: 13962–13967. 10.1073/pnas.0606384103 PubMed DOI PMC

Corrigan RM, Bellows LE, Wood A, Gründling A. ppGpp negatively impacts ribosome assembly affecting growth and antimicrobial tolerance in Gram-positive bacteria. Proc Natl Acad Sci USA. 2016;113: E1710–1719. 10.1073/pnas.1522179113 PubMed DOI PMC

Steinchen W, Bange G. The magic dance of the alarmones (p)ppGpp: The structural biology of the alarmones (p)ppGpp. Molecular Microbiology. 2016;101: 531–544. PubMed

Vinogradova DS, Zegarra V, Maksimova E, Nakamoto JA, Kasatsky P, Paleskava A, et al. How the initiating ribosome copes with ppGpp to translate mRNAs. PLoS Biol. 2020;18: e3000593 10.1371/journal.pbio.3000593 PubMed DOI PMC

Kanjee U, Ogata K, Houry WA. Direct binding targets of the stringent response alarmone (p)ppGpp: Protein targets of ppGpp. Molecular Microbiology. 2012;85: 1029–1043. 10.1111/j.1365-2958.2012.08177.x PubMed DOI

Zhang Y, Zborníková E, Rejman D, Gerdes K. Novel (p)ppGpp Binding and Metabolizing Proteins of Escherichia coli. MBio. 2018;9 10.1128/mBio.02188-17 PubMed DOI PMC

Wang B, Dai P, Ding D, Del Rosario A, Grant RA, Pentelute BL, et al. Affinity-based capture and identification of protein effectors of the growth regulator ppGpp. Nat Chem Biol. 2019;15: 141–150. 10.1038/s41589-018-0183-4 PubMed DOI PMC

Bokinsky G, Baidoo EEK, Akella S, Burd H, Weaver D, Alonso-Gutierrez J, et al. HipA-triggered growth arrest and β-lactam tolerance in Escherichia coli are mediated by RelA-dependent ppGpp synthesis. J Bacteriol. 2013;195: 3173–3182. 10.1128/JB.02210-12 PubMed DOI PMC

Dalebroux ZD, Swanson MS. ppGpp: magic beyond RNA polymerase. Nat Rev Microbiol. 2012;10: 203–212. 10.1038/nrmicro2720 PubMed DOI

Mostertz J, Scharf C, Hecker M, Homuth G. Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. Microbiology (Reading, Engl). 2004;150: 497–512. PubMed

Hantke I, Schäfer H, Janczikowski A, Turgay K. YocM a small heat shock protein can protect Bacillus subtilis cells during salt stress. Mol Microbiol. 2019;111: 423–440. 10.1111/mmi.14164 PubMed DOI

Gaca AO, Kudrin P, Colomer-Winter C, Beljantseva J, Liu K, Anderson B, et al. From (p)ppGpp to (pp)pGpp: Characterization of Regulatory Effects of pGpp Synthesized by the Small Alarmone Synthetase of Enterococcus faecalis. J Bacteriol. 2015;197: 2908–2919. 10.1128/JB.00324-15 PubMed DOI PMC

Hecker M, Völker U, Heim C. RelA-independent (p)ppGpp accumulation and heat shock protein induction after salt stress in Bacillus subtilis. FEMS Microbiology Letters. 1989;58: 125–128. 10.1111/j.1574-6968.1989.tb03031.x DOI

Pöther D-C, Liebeke M, Hochgräfe F, Antelmann H, Becher D, Lalk M, et al. Diamide triggers mainly S Thiolations in the cytoplasmic proteomes of Bacillus subtilis and Staphylococcus aureus. J Bacteriol. 2009;191: 7520–7530. 10.1128/JB.00937-09 PubMed DOI PMC

Drzewiecki K, Eymann C, Mittenhuber G, Hecker M. The yvyD gene of Bacillus subtilis is under dual control of sigmaB and sigmaH. J Bacteriol. 1998;180: 6674–6680. PubMed PMC

Tagami K, Nanamiya H, Kazo Y, Maehashi M, Suzuki S, Namba E, et al. Expression of a small (p)ppGpp synthetase, YwaC, in the (p)ppGpp(0) mutant of Bacillus subtilis triggers YvyD-dependent dimerization of ribosome. Microbiologyopen. 2012;1: 115–134. 10.1002/mbo3.16 PubMed DOI PMC

Cashel M. The Control of Ribonucleic Acid Synthesis in Escherichia coli : IV. RELEVANCE OF UNUSUAL PHOSPHORYLATED COMPOUNDS FROM AMINO ACID-STARVED STRINGENT STRAINS. Journal of Biological Chemistry. 1969;244: 3133–3141. PubMed

Schreiber G, Metzger S, Aizenman E, Roza S, Cashel M, Glaser G. Overexpression of the relA gene in Escherichia coli. J Biol Chem. 1991;266: 3760–3767. PubMed

Nouri H, Monnier A-F, Fossum-Raunehaug S, Maciag-Dorszynska M, Cabin-Flaman A, Képès F, et al. Multiple links connect central carbon metabolism to DNA replication initiation and elongation in Bacillus subtilis. DNA Res. 2018. 10.1093/dnares/dsy031 PubMed DOI PMC

Lopez JM, Marks CL, Freese E. The decrease of guanine nucleotides initiates sporulation of Bacillus subtilis. Biochim Biophys Acta. 1979;587: 238–252. 10.1016/0304-4165(79)90357-x PubMed DOI

Tojo S, Satomura T, Kumamoto K, Hirooka K, Fujita Y. Molecular Mechanisms Underlying the Positive Stringent Response of the Bacillus subtilis ilv-leu Operon, Involved in the Biosynthesis of Branched-Chain Amino Acids. J Bacteriol. 2008;190: 6134–6147. 10.1128/JB.00606-08 PubMed DOI PMC

Tojo S, Kumamoto K, Hirooka K, Fujita Y. Heavy involvement of stringent transcription control depending on the adenine or guanine species of the transcription initiation site in glucose and pyruvate metabolism in Bacillus subtilis. J Bacteriol. 2010;192: 1573–1585. 10.1128/JB.01394-09 PubMed DOI PMC

Kriel A, Brinsmade SR, Tse JL, Tehranchi AK, Bittner AN, Sonenshein AL, et al. GTP Dysregulation in Bacillus subtilis Cells Lacking (p)ppGpp Results in Phenotypic Amino Acid Auxotrophy and Failure To Adapt to Nutrient Downshift and Regulate Biosynthesis Genes. Journal of Bacteriology. 2014;196: 189–201. 10.1128/JB.00918-13 PubMed DOI PMC

Eymann C, Homuth G, Scharf C, Hecker M. Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis. J Bacteriol. 2002;184: 2500–2520. 10.1128/JB.184.9.2500-2520.2002 PubMed DOI PMC

Zhang S, Haldenwang WG. RelA is a component of the nutritional stress activation pathway of the Bacillus subtilis transcription factor sigma B. J Bacteriol. 2003;185: 5714–5721. 10.1128/JB.185.19.5714-5721.2003 PubMed DOI PMC

Zhang S, Haldenwang WG. Contributions of ATP, GTP, and redox state to nutritional stress activation of the Bacillus subtilis sigmaB transcription factor. J Bacteriol. 2005;187: 7554–7560. 10.1128/JB.187.22.7554-7560.2005 PubMed DOI PMC

Molière N, Hoßmann J, Schäfer H, Turgay K. Role of Hsp100/Clp Protease Complexes in Controlling the Regulation of Motility in Bacillus subtilis. Front Microbiol. 2016;7: 315 10.3389/fmicb.2016.00315 PubMed DOI PMC

Paget MSB, Molle V, Cohen G, Aharonowitz Y, Buttner MJ. Defining the disulphide stress response in Streptomyces coelicolor A3(2): identification of the sigmaR regulon. Molecular Microbiology. 2001;42: 1007–1020. 10.1046/j.1365-2958.2001.02675.x PubMed DOI

Gaca AO, Abranches J, Kajfasz JK, Lemos JA. Global transcriptional analysis of the stringent response in Enterococcus faecalis. Microbiology (Reading, Engl). 2012;158: 1994–2004. PubMed PMC

Schmidt EK, Clavarino G, Ceppi M, Pierre P. SUnSET, a nonradioactive method to monitor protein synthesis. Nat Methods. 2009;6: 275–277. 10.1038/nmeth.1314 PubMed DOI

Svitil AL, Cashel M, Zyskind JW. Guanosine tetraphosphate inhibits protein synthesis in vivo. A possible protective mechanism for starvation stress in Escherichia coli. J Biol Chem. 1993;268: 2307–2311. PubMed

Diez S, Ryu J, Caban K, Gonzalez RL, Dworkin J. (p)ppGpp directly regulates translation initiation during entry into quiescence. bioRxiv. 2019; 807917 10.1101/807917 PubMed DOI PMC

Zhang S, Scott JM, Haldenwang WG. Loss of ribosomal protein L11 blocks stress activation of the Bacillus subtilis transcription factor sigma(B). J Bacteriol. 2001;183: 2316–2321. 10.1128/JB.183.7.2316-2321.2001 PubMed DOI PMC

Beckert B, Abdelshahid M, Schäfer H, Steinchen W, Arenz S, Berninghausen O, et al. Structure of the Bacillus subtilis hibernating 100S ribosome reveals the basis for 70S dimerization. EMBO J. 2017;36: 2061–2072. 10.15252/embj.201696189 PubMed DOI PMC

Trinquier A, Ulmer JE, Gilet L, Figaro S, Hammann P, Kuhn L, et al. tRNA Maturation Defects Lead to Inhibition of rRNA Processing via Synthesis of pppGpp. Molecular Cell. 2019;0 10.1016/j.molcel.2019.03.030 PubMed DOI

Engman J, von Wachenfeldt C. Regulated protein aggregation: a mechanism to control the activity of the ClpXP adaptor protein YjbH. Mol Microbiol. 2015;95: 51–63. 10.1111/mmi.12842 PubMed DOI

Fitzsimmons LF, Liu L, Kim J-S, Jones-Carson J, Vázquez-Torres A. Salmonella Reprograms Nucleotide Metabolism in Its Adaptation to Nitrosative Stress. Aballay A, editor. mBio. 2018;9: e00211–18. 10.1128/mBio.00211-18 PubMed DOI PMC

Hyduke DR, Jarboe LR, Tran LM, Chou KJY, Liao JC. Integrated network analysis identifies nitric oxide response networks and dihydroxyacid dehydratase as a crucial target in Escherichia coli. Proceedings of the National Academy of Sciences. 2007;104: 8484–8489. 10.1073/pnas.0610888104 PubMed DOI PMC

Richardson AR, Payne EC, Younger N, Karlinsey JE, Thomas VC, Becker LA, et al. Multiple Targets of Nitric Oxide in the Tricarboxylic Acid Cycle of Salmonella enterica Serovar Typhimurium. Cell Host & Microbe. 2011;10: 33–43. 10.1016/j.chom.2011.06.004 PubMed DOI PMC

Gallant J, Palmer L, Pao CC. Anomalous synthesis of ppGpp in growing cells. Cell. 1977;11: 181–185. 10.1016/0092-8674(77)90329-4 PubMed DOI

Katz A, Orellana O. Protein Synthesis and the Stress Response. In: Biyani M, editor. Cell-Free Protein Synthesis. InTech; 2012.

Kramer GF, Baker JC, Ames BN. Near-UV stress in Salmonella typhimurium: 4-thiouridine in tRNA, ppGpp, and ApppGpp as components of an adaptive response. J Bacteriol. 1988;170: 2344–2351. 10.1128/jb.170.5.2344-2351.1988 PubMed DOI PMC

Hahn J, Tanner AW, Carabetta VJ, Cristea IM, Dubnau D. ComGA-RelA interaction and persistence in the Bacillus subtilis K-state. Mol Microbiol. 2015;97: 454–471. 10.1111/mmi.13040 PubMed DOI PMC

Scott JM, Haldenwang WG. Obg, an essential GTP binding protein of Bacillus subtilis, is necessary for stress activation of transcription factor sigma(B). J Bacteriol. 1999;181: 4653–4660. PubMed PMC

Bruel N, Castanié-Cornet M-P, Cirinesi A-M, Koningstein G, Georgopoulos C, Luirink J, et al. Hsp33 controls elongation factor-Tu stability and allows Escherichia coli growth in the absence of the major DnaK and trigger factor chaperones. J Biol Chem. 2012;287: 44435–44446. 10.1074/jbc.M112.418525 PubMed DOI PMC

Maaβ S, Wachlin G, Bernhardt J, Eymann C, Fromion V, Riedel K, et al. Highly precise quantification of protein molecules per cell during stress and starvation responses in Bacillus subtilis. Mol Cell Proteomics. 2014;13: 2260–2276. 10.1074/mcp.M113.035741 PubMed DOI PMC

Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011;334: 1081–1086. 10.1126/science.1209038 PubMed DOI

Rallu F, Gruss A, Ehrlich SD, Maguin E. Acid- and multistress-resistant mutants of Lactococcus lactis: identification of intracellular stress signals. Molecular Microbiology. 2000;35: 517–528. 10.1046/j.1365-2958.2000.01711.x PubMed DOI

VanBogelen RA, Kelley PM, Neidhardt FC. Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J Bacteriol. 1987;169: 26–32. 10.1128/jb.169.1.26-32.1987 PubMed DOI PMC

Abranches J, Martinez AR, Kajfasz JK, Chávez V, Garsin DA, Lemos JA. The molecular alarmone (p)ppGpp mediates stress responses, vancomycin tolerance, and virulence in Enterococcus faecalis. J Bacteriol. 2009;191: 2248–2256. 10.1128/JB.01726-08 PubMed DOI PMC

Okada Y, Makino S, Tobe T, Okada N, Yamazaki S. Cloning of rel from Listeria monocytogenes as an osmotolerance involvement gene. Appl Environ Microbiol. 2002;68: 1541–1547. 10.1128/AEM.68.4.1541-1547.2002 PubMed DOI PMC

Yang X, Ishiguro EE. Temperature-Sensitive Growth and Decreased Thermotolerance Associated with relA Mutations in Escherichia coli. J Bacteriol. 2003;185: 5765–5771. 10.1128/JB.185.19.5765-5771.2003 PubMed DOI PMC

Khakimova M, Ahlgren HG, Harrison JJ, English AM, Nguyen D. The stringent response controls catalases in Pseudomonas aeruginosa and is required for hydrogen peroxide and antibiotic tolerance. J Bacteriol. 2013;195: 2011–2020. 10.1128/JB.02061-12 PubMed DOI PMC

Sambrook J, Russell DW. Molecular cloning: a laboratory manual. 3rd ed Cold Spring Harbor, N.Y: Cold Spring Harbor Laboratory Press; 2001.

Spizizen J. TRANSFORMATION OF BIOCHEMICALLY DEFICIENT STRAINS OF BACILLUS SUBTILIS BY DEOXYRIBONUCLEATE. Proc Natl Acad Sci USA. 1958;44: 1072–1078. 10.1073/pnas.44.10.1072 PubMed DOI PMC

Nakano MM, Zhu Y, Liu J, Reyes DY, Yoshikawa H, Zuber P. Mutations conferring amino acid residue substitutions in the carboxy-terminal domain of RNA polymerase alpha can suppress clpX and clpP with respect to developmentally regulated transcription in Bacillus subtilis. Mol Microbiol. 2000;37: 869–884. 10.1046/j.1365-2958.2000.02052.x PubMed DOI

Arnaud M, Chastanet A, Débarbouillé M. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol. 2004;70: 6887–6891. 10.1128/AEM.70.11.6887-6891.2004 PubMed DOI PMC

Stülke J, Hanschke R, Hecker M. Temporal activation of beta-glucanase synthesis in Bacillus subtilis is mediated by the GTP pool. J Gen Microbiol. 1993;139: 2041–2045. 10.1099/00221287-139-9-2041 PubMed DOI

Lamy M-C, Zouine M, Fert J, Vergassola M, Couve E, Pellegrini E, et al. CovS/CovR of group B streptococcus: a two-component global regulatory system involved in virulence: The CovS/CovR regulatory system of Streptococcus agalactiae. Molecular Microbiology. 2004;54: 1250–1268. 10.1111/j.1365-2958.2004.04365.x PubMed DOI

Nuss AM, Heroven AK, Waldmann B, Reinkensmeier J, Jarek M, Beckstette M, et al. Transcriptomic Profiling of Yersinia pseudotuberculosis Reveals Reprogramming of the Crp Regulon by Temperature and Uncovers Crp as a Master Regulator of Small RNAs. Sharma CM, editor. Genet PLoS. 2015;11: e1005087 10.1371/journal.pgen.1005087 PubMed DOI PMC

Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9: 357–359. 10.1038/nmeth.1923 PubMed DOI PMC

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25: 2078–2079. 10.1093/bioinformatics/btp352 PubMed DOI PMC

Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11: R106 10.1186/gb-2010-11-10-r106 PubMed DOI PMC

Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30: 207–210. 10.1093/nar/30.1.207 PubMed DOI PMC

Dugar G, Herbig A, Förstner KU, Heidrich N, Reinhardt R, Nieselt K, et al. High-Resolution Transcriptome Maps Reveal Strain-Specific Regulatory Features of Multiple Campylobacter jejuni Isolates. Hughes D, editor. PLoS Genetics. 2013;9: e1003495 10.1371/journal.pgen.1003495 PubMed DOI PMC

Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA. 1979;76: 4350–4354. 10.1073/pnas.76.9.4350 PubMed DOI PMC

Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227: 680–685. 10.1038/227680a0 PubMed DOI

Neuhoff V, Arold N, Taube D, Ehrhardt W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis. 1988;9: 255–262. 10.1002/elps.1150090603 PubMed DOI

Yarmolinsky MB, Haba GL. INHIBITION BY PUROMYCIN OF AMINO ACID INCORPORATION INTO PROTEIN. Proc Natl Acad Sci USA. 1959;45: 1721–1729. 10.1073/pnas.45.12.1721 PubMed DOI PMC

Nathans D. PUROMYCIN INHIBITION OF PROTEIN SYNTHESIS: INCORPORATION OF PUROMYCIN INTO PEPTIDE CHAINS. Proc Natl Acad Sci USA. 1964;51: 585–592. 10.1073/pnas.51.4.585 PubMed DOI PMC

Krüger E, Witt E, Ohlmeier S, Hanschke R, Hecker M. The clp proteases of Bacillus subtilis are directly involved in degradation of misfolded proteins. J Bacteriol. 2000;182: 3259–3265. 10.1128/jb.182.11.3259-3265.2000 PubMed DOI PMC

Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9: 676–682. 10.1038/nmeth.2019 PubMed DOI PMC

Ihara Y, Ohta H, Masuda S. A highly sensitive quantification method for the accumulation of alarmone ppGpp in Arabidopsis thaliana using UPLC-ESI-qMS/MS. J Plant Res. 2015;128: 511–518. 10.1007/s10265-015-0711-1 PubMed DOI

Steinchen W, Schuhmacher JS, Altegoer F, Fage CD, Srinivasan V, Linne U, et al. Catalytic mechanism and allosteric regulation of an oligomeric (p)ppGpp synthetase by an alarmone. Proc Natl Acad Sci USA. 2015;112: 13348–13353. 10.1073/pnas.1505271112 PubMed DOI PMC

Hughes CS, Moggridge S, Müller T, Sorensen PH, Morin GB, Krijgsveld J. Single-pot, solid-phase-enhanced sample preparation for proteomics experiments. Nat Protoc. 2019;14: 68–85. 10.1038/s41596-018-0082-x PubMed DOI

Plubell DL, Wilmarth PA, Zhao Y, Fenton AM, Minnier J, Reddy AP, et al. Extended Multiplexing of Tandem Mass Tags (TMT) Labeling Reveals Age and High Fat Diet Specific Proteome Changes in Mouse Epididymal Adipose Tissue. Mol Cell Proteomics. 2017;16: 873–890. 10.1074/mcp.M116.065524 PubMed DOI PMC

Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu DJ, et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019;47: D442–D450. 10.1093/nar/gky1106 PubMed DOI PMC

Zhu B, Stülke J. SubtiWiki in 2018: from genes and proteins to functional network annotation of the model organism Bacillus subtilis. Nucleic Acids Research. 2018;46: D743–D748. 10.1093/nar/gkx908 PubMed DOI PMC

R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2018. https://www.R-project.org/

Yu G, Wang L-G, Han Y, He Q-Y. clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters. OMICS: A Journal of Integrative Biology. 2012;16: 284–287. 10.1089/omi.2011.0118 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...