PpGpp negatively impacts ribosome assembly affecting growth and antimicrobial tolerance in Grampositive bacteria

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 12, 2016, Pages E1710-E1719

  Corrigan, Rebecca M ^a   Bellows, Lauren E ^b   Wood, Alison ^a   Gründling, Angelika ^b  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

ppGpp; Ribosome; Staphylococcus aureus; Stringent response; Tolerance

Indexed keywords

BACTERIAL ENZYME; GMK ENZYME; GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; GUANOSINE 3' DIPHOSPHATE 5' TRIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ERA; GUANOSINE TRIPHOSPHATASE HFLX; GUANOSINE TRIPHOSPHATASE OBGE; GUANOSINE TRIPHOSPHATASE RBGA; GUANOSINE TRIPHOSPHATASE RSGA; GUANOSINE TRIPHOSPHATE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; NUCLEOTIDE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; PROTEIN BINDING;

ANTIBIOTIC RESISTANCE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; BINDING AFFINITY; CONTROLLED STUDY; ENTEROCOCCUS FAECALIS; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; GRAM POSITIVE BACTERIUM; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; RIBOSOME; STAPHYLOCOCCUS AUREUS; BIOSYNTHESIS; DRUG EFFECTS; ESCHERICHIA COLI; GENE LIBRARY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SCREENING; METABOLISM; MICROBIAL SENSITIVITY TEST; OPEN READING FRAME; ORGANELLE BIOGENESIS; PHYSIOLOGY; ULTRASTRUCTURE;

ANTI-BACTERIAL AGENTS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; GENE LIBRARY; GTP PHOSPHOHYDROLASES; GUANOSINE TETRAPHOSPHATE; GUANOSINE TRIPHOSPHATE; HIGH-THROUGHPUT SCREENING ASSAYS; MICROBIAL SENSITIVITY TESTS; OPEN READING FRAMES; ORGANELLE BIOGENESIS; PROTEIN BINDING; RIBOSOMES; STAPHYLOCOCCUS AUREUS;

EID: 84962305197     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1522179113     Document Type: Article

References (77)

1. Battesti A, Bouveret E (2006) Acyl carrier protein/SpoT interaction, the switch linking SpoT-dependent stress response to fatty acid metabolism. Mol Microbiol 62(4): 1048-1063.
2. Cashel M (1969) The control of ribonucleic acid synthesis in Escherichia coli. IV. Relevance of unusual phosphorylated compounds from amino acid-starved stringent strains. J Biol Chem 244(12):3133-3141.
3. Cashel M, Gentry DR, Hernandez VJ, Vinella D, eds (1996) The Stringent Response (ASM, Washington, DC), Vol 1, pp 1458-1496.
4. Potrykus K, Cashel M (2008) (p)ppGpp: Still magical? Annu Rev Microbiol 62:35-51.
5. Lemos JA, Brown TA, Jr, Burne RA (2004) Effects of RelA on key virulence properties of planktonic and biofilm populations of Streptococcus mutans. Infect Immun 72(3): 1431-1440.
6. Nguyen D, et al. (2011) Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334(6058):982-986.
7. Ochi K, Kandala JC, Freese E (1981) Initiation of Bacillus subtilis sporulation by the stringent response to partial amino acid deprivation. J Biol Chem 256(13):6866-6875.
8. Potrykus K, Murphy H, Philippe N, Cashel M (2011) ppGpp is the major source of growth rate control in E. coli. Environ Microbiol 13(3):563-575.
9. Maisonneuve E, Castro-Camargo M, Gerdes K (2013) (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154(5):1140-1150.
10. Avarbock D, Avarbock A, Rubin H (2000) Differential regulation of opposing RelMtb activities by the aminoacylation state of a tRNA ribosome mRNA RelMtb complex. Biochemistry 39(38):11640-11648.
11. Gropp M, Strausz Y, Gross M, Glaser G (2001) Regulation of Escherichia coli RelA requires oligomerization of the C-terminal domain. J Bacteriol 183(2):570-579.
12. Haseltine WA, Block R (1973) 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 70(5):1564-1568.
13. Ramagopal S, Davis BD (1974) Localization of the stringent protein of Escherichia coli on the 50S ribosomal subunit. Proc Natl Acad Sci USA 71(3):820-824.
14. Magnusson LU, Farewell A, Nyström T (2005) ppGpp: A global regulator in Escherichia coli. Trends Microbiol 13(5):236-242.
15. Buglino J, Shen V, Hakimian P, Lima CD (2002) Structural and biochemical analysis of the Obg GTP binding protein. Structure 10(11):1581-1592.
16. Kanjee U, Ogata K, Houry WA (2012) Direct binding targets of the stringent response alarmone (p)ppGpp. Mol Microbiol 85(6):1029-1043.
17. Maciag M, Kochanowska M, Lyzeń R, Wegrzyn G, Szalewska-Palasz A (2010) ppGpp inhibits the activity of Escherichia coli DnaG primase. Plasmid 63(1):61-67.
18. Gentry D, Li T, Rosenberg M, McDevitt D (2000) The rel gene is essential for in vitro growth of Staphylococcus aureus. J Bacteriol 182(17):4995-4997.
19. Nanamiya H, et al. (2008) Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis. Mol Microbiol 67(2):291-304.
20. Geiger T, et al. (2010) Role of the (p)ppGpp synthase RSH, a RelA/SpoT homolog, in stringent response and virulence of Staphylococcus aureus. Infect Immun 78(5): 1873-1883.
21. Geiger T, Kästle B, Gratani FL, Goerke C, Wolz C (2014) Two small (p)ppGpp synthases in Staphylococcus aureus mediate tolerance against cell envelope stress conditions. J Bacteriol 196(4):894-902.
22. Gao W, et al. (2013) The RpoB H481Y rifampicin resistance mutation and an active stringent response reduce virulence and increase resistance to innate immune responses in Staphylococcus aureus. J Infect Dis 207(6):929-939.
23. Gao W, et al. (2010) Two novel point mutations in clinical Staphylococcus aureus reduce linezolid susceptibility and switch on the stringent response to promote persistent infection. PLoS Pathog 6(6):e1000944.
24. Geiger T, et al. (2012) The stringent response of Staphylococcus aureus and its impact on survival after phagocytosis through the induction of intracellular PSMs expression. PLoS Pathog 8(11):e1003016.
25. MwangiMM, et al. (2013) Whole-genome sequencing reveals a link between β-lactam resistance and synthetases of the alarmone (p)ppGpp in Staphylococcus aureus. Microb Drug Resist 19(3):153-159.
26. Krásný L, Gourse RL (2004) An alternative strategy for bacterial ribosome synthesis: Bacillus subtilis rRNA transcription regulation. EMBO J 23(22):4473-4483.
27. Bittner AN, Kriel A, Wang JD (2014) Lowering GTP level increases survival of amino acid starvation but slows growth rate for Bacillus subtilis cells lacking (p)ppGpp. J Bacteriol 196(11):2067-2076.
28. Kriel A, et al. (2012) Direct regulation of GTP homeostasis by (p)ppGpp: A critical component of viability and stress resistance. Mol Cell 48(2):231-241.
29. Gaca AO, et al. (2013) Basal levels of (p)ppGpp in Enterococcus faecalis: The magic beyond the stringent response. MBio 4(5):e00646-e13.
30. Liu K, et al. (2015) Molecular mechanism and evolution of guanylate kinase regulation by (p)ppGpp. Mol Cell 57(4):735-749.
31. Handke LD, Shivers RP, Sonenshein AL (2008) Interaction of Bacillus subtilis CodY with GTP. J Bacteriol 190(3):798-806.
32. Corrigan RM, et al. (2013) Systematic identification of conserved bacterial c-di-AMP receptor proteins. Proc Natl Acad Sci USA 110(22):9084-9089.
33. Roelofs KG, Wang J, Sintim HO, Lee VT (2011) Differential radial capillary action of ligand assay for high-throughput detection of protein-metabolite interactions. Proc Natl Acad Sci USA 108(37):15528-15533.
34. Campbell TL, Henderson J, Heinrichs DE, Brown ED (2006) The yjeQ gene is required for virulence of Staphylococcus aureus. Infect Immun 74(8):4918-4921.
35. Campbell TL, Daigle DM, Brown ED (2005) Characterization of the Bacillus subtilis GTPase YloQ and its role in ribosome function. Biochem J 389(Pt 3):843-852.
36. Himeno H, et al. (2004) A novel GTPase activated by the small subunit of ribosome. Nucleic Acids Res 32(17):5303-5309.
37. Anderson PE, Matsunaga J, Simons EL, Simons RW (1996) Structure and regulation of the Salmonella typhimurium rnc-era-recO operon. Biochimie 78(11-12):1025-1034.
38. Gollop N, March PE (1991) A GTP-binding protein (Era) has an essential role in growth rate and cell cycle control in Escherichia coli. J Bacteriol 173(7):2265-2270.
39. March PE, Lerner CG, Ahnn J, Cui X, Inouye M (1988) The Escherichia coli Ras-like protein (Era) has GTPase activity and is essential for cell growth. Oncogene 2(6): 539-544.
40. Gulati M, Jain N, Anand B, Prakash B, Britton RA (2013) Mutational analysis of the ribosome assembly GTPase RbgA provides insight into ribosome interaction and ribosome- stimulated GTPase activation. Nucleic Acids Res 41(5):3217-3227.
41. Morimoto T, et al. (2002) Six GTP-binding proteins of the Era/Obg family are essential for cell growth in Bacillus subtilis. Microbiology 148(Pt 11):3539-3552.
42. Uicker WC, Schaefer L, Britton RA (2006) The essential GTPase RbgA (YlqF) is required for 50S ribosome assembly in Bacillus subtilis. Mol Microbiol 59(2):528-540.
43. Sayed A, Matsuyama Si, Inouye M (1999) Era, an essential Escherichia coli small G-protein, binds to the 30S ribosomal subunit. Biochem Biophys Res Commun 264(1): 51-54.
44. Sharma MR, et al. (2005) Interaction of Era with the 30S ribosomal subunit implications for 30S subunit assembly. Mol Cell 18(3):319-329.
45. Jomaa A, et al. (2011) Understanding ribosome assembly: The structure of in vivo assembled immature 30S subunits revealed by cryo-electron microscopy. RNA 17(4): 697-709.
46. Hase Y, Yokoyama S, Muto A, Himeno H (2009) Removal of a ribosome small subunitdependent GTPase confers salt resistance on Escherichia coli cells. RNA 15(9):1766-1774.
47. Gulati M, Jain N, Davis JH, Williamson JR, Britton RA (2014) Functional interaction between ribosomal protein L6 and RbgA during ribosome assembly. PLoS Genet 10(10):e1004694.
48. Matsuo Y, et al. (2006) The GTP-binding protein YlqF participates in the late step of 50 S ribosomal subunit assembly in Bacillus subtilis. J Biol Chem 281(12):8110-8117.
49. Jain N, et al. (2009) E. coli HflX interacts with 50S ribosomal subunits in presence of nucleotides. Biochem Biophys Res Commun 379(2):201-205.
50. Zhang Y, et al. (2015) HflX is a ribosome-splitting factor rescuing stalled ribosomes under stress conditions. Nat Struct Mol Biol 22(11):906-913.
51. Daigle DM, Brown ED (2004) Studies of the interaction of Escherichia coli YjeQ with the ribosome in vitro. J Bacteriol 186(5):1381-1387.
52. Cashel M (1975) Regulation of bacterial ppGpp and pppGpp. Annu Rev Microbiol 29: 301-318.
53. Kästle B, et al. (2015) rRNA regulation during growth and under stringent conditions in Staphylococcus aureus. Environ Microbiol 17(11):4394-4405.
54. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S (2004) Bacterial persistence as a phenotypic switch. Science 305(5690):1622-1625.
55. Levin BR, Rozen DE (2006) Non-inherited antibiotic resistance. Nat Rev Microbiol 4(7): 556-562.
56. Feng B, et al. (2014) Structural and functional insights into the mode of action of a universally conserved Obg GTPase. PLoS Biol 12(5):e1001866.
57. Rojas AM, Ehrenberg M, Andersson SG, Kurland CG (1984) ppGpp inhibition of elongation factors Tu, G and Ts during polypeptide synthesis. Mol Gen Genet 197(1): 36-45.
58. Miller DL, Cashel M, Weissbach H (1973) The interaction of guanosine 5′-diphosphate, 2′ (3′)-diphosphate with the bacterial elongation factor Tu. Arch Biochem Biophys 154(2):675-682.
59. Legault L, Jeantet C, Gros F (1972) Inhibition of in vitro protein synthesis by ppGpp. FEBS Lett 27(1):71-75.
60. Foti JJ, Schienda J, Sutera VA, Jr, Lovett ST (2005) A bacterial G protein-mediated response to replication arrest. Mol Cell 17(4):549-560.
61. Wout P, et al. (2004) The Escherichia coli GTPase CgtAE cofractionates with the 50S ribosomal subunit and interacts with SpoT, a ppGpp synthetase/hydrolase. J Bacteriol 186(16):5249-5257.
62. Paul BJ, et al. (2004) DksA: A critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP. Cell 118(3):311-322.
63. Ross W, Vrentas CE, Sanchez-Vazquez P, Gaal T, Gourse RL (2013) The magic spot: A ppGpp binding site on E. coli RNA polymerase responsible for regulation of transcription initiation. Mol Cell 50(3):420-429.
64. Achila D, Gulati M, Jain N, Britton RA (2012) Biochemical characterization of ribosome assembly GTPase RbgA in Bacillus subtilis. J Biol Chem 287(11):8417-8423.
65. Merlie JP, Pizer LI (1973) Regulation of phospholipid synthesis in Escherichia coli by guanosine tetraphosphate. J Bacteriol 116(1):355-366.
66. Wang JD, Sanders GM, Grossman AD (2007) Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128(5):865-875.
67. Gründling A, Schneewind O (2007a) Genes required for glycolipid synthesis and lipoteichoic acid anchoring in Staphylococcus aureus. J Bacteriol 189(6):2521-2530.
68. Corrigan RM, Abbott JC, Burhenne H, Kaever V, Gründling A (2011) c-di-AMP is a new second messenger in Staphylococcus aureus with a role in controlling cell size and envelope stress. PLoS Pathog 7(9):e1002217.
69. Lu D, et al. (2009) Structure-based mechanism of lipoteichoic acid synthesis by Staphylococcus aureus LtaS. Proc Natl Acad Sci USA 106(5):1584-1589.
70. Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166(4):557-580.
71. Guyer MS, Reed RR, Steitz JA, Low KB (1981) Identification of a sex-factor-affinity site in E. coli as gamma delta. Cold Spring Harb Symp Quant Biol 45(Pt 1):135-140.
72. Monk IR, Shah IM, Xu M, Tan MW, Foster TJ (2012) Transforming the untransformable: Application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. MBio 3(2):e00277-11.
73. Lee VT, et al. (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65(6):1474-1484.
74. Mechold U, Potrykus K, Murphy H, Murakami KS, Cashel M (2013) Differential regulation by ppGpp versus pppGpp in Escherichia coli. Nucleic Acids Res 41(12): 6175-6189.
75. Boles BR, Thoendel M, Roth AJ, Horswill AR (2010) Identification of genes involved in polysaccharide-independent Staphylococcus aureus biofilm formation. PLoS One 5(4): e10146.
76. Burkholder PR, Giles NH, Jr (1947) Induced biochemical mutations in Bacillus subtilis. Am J Bot 34(6):345-348.
77. Jacob AE, Hobbs SJ (1974) Conjugal transfer of plasmid-borne multiple antibiotic resistance in Streptococcus faecalis var. zymogenes. J Bacteriol 117(2):360-372.