Basal levels of (p)ppGpp in Enterococcus faecalis: The magic beyond the stringent response

mBio

Volumn 4, Issue 5, 2013, Pages

  Gaca, Anthony O ^a   Kajfasz, Jessica K ^a   Miller, James H ^a   Liu, Kuanqing ^b   Wang, Jue D ^b   Abranches, Jacqueline ^a   Lemos, José A ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALARMONE; BACTERIAL PROTEIN; HYDROGEN PEROXIDE; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACILLUS SUBTILIS; BACTERIAL METABOLISM; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BIOSYNTHESIS; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENERGY YIELD; ENTEROCOCCUS FAECALIS; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; ENZYME SYNTHESIS; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENE IDENTIFICATION; METABOLIC BALANCE; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; SIGNAL TRANSDUCTION; STRINGENT RESPONSE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; ENERGY METABOLISM; ENTEROCOCCUS FAECALIS; FERMENTATION; GUANINE NUCLEOTIDES; GUANOSINE TRIPHOSPHATE; HYDROGEN PEROXIDE; STRESS, PHYSIOLOGICAL;

EID: 84887198561     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00646-13     Document Type: Article

References (67)

1. Arias CA, Murray BE. 2012. The rise of the Enterococcus: beyond vancomycin resistance. Nat. Rev. Microbiol. 10:266-278.
2. Murray BE. 1990. The life and times of the Enterococcus. Clin. Microbiol. Rev. 3:46-65.
3. Potrykus K, Cashel M. 2008. (p)ppGpp: still magical? Annu. Rev. Microbiol. 62:35-51.
4. Lemos JA, Nascimento MM, Lin VK, Abranches J, Burne RA. 2008. Global regulation by (p)ppGpp and CodY in Streptococcus mutans. J. Bacteriol. 190:5291-5299.
5. Gaca AO, Abranches J, Kajfasz JK, Lemos JA. 2012. Global transcriptional analysis of the stringent response in Enterococcus faecalis. Microbiology 158:1994-2004.
6. Traxler MF, Summers SM, Nguyen HT, Zacharia VM, Hightower GA, Smith JT, Conway T. 2008. The global, ppGpp-mediated stringent response to amino acid starvation in Escherichia coli. Mol. Microbiol. 68: 1128-1148.
7. Geiger T, Goerke C, Fritz M, Schäfer T, Ohlsen K, Liebeke M, Lalk M, Wolz C. 2010. Role of the (p)ppGpp synthase RSH, a RelA/SpoT homolog, in stringent response and virulence of Staphylococcus aureus. Infect. Immun. 78:1873-1883.
8. Krásný L, Gourse RL. 2004. An alternative strategy for bacterial ribosome synthesis: Bacillus subtilis rRNA transcription regulation. EMBO J. 23: 4473-4483.
9. Vrentas CE, Gaal T, Berkmen MB, Rutherford ST, Haugen SP, Vassylyev DG, Ross W, Gourse RL. 2008. Still looking for the magic spot: the crystallographically defined binding site for ppGpp on RNA polymerase is unlikely to be responsible for rRNA transcription regulation. J. Mol. Biol. 377:551-564.
10. Kuroda A, Murphy H, Cashel M, Kornberg A. 1997. Guanosine tetraand pentaphosphate promote accumulation of inorganic polyphosphate in Escherichia coli. J. Biol. Chem. 272:21240-21243.
11. Kriel A, Bittner AN, Kim SH, Liu K, Tehranchi AK, Zou WY, Rendon S, Chen R, Tu BP, Wang JD. 2012. Direct regulation of GTP homeostasis by (p)ppGpp: a critical component of viability and stress resistance. Mol. Cell 48:231-241.
12. Wang JD, Sanders GM, Grossman AD. 2007. Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128:865-875.
13. Xiao H, Kalman M, Ikehara K, Zemel S, Glaser G, Cashel M. 1991. Residual guanosine 3=,5=-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J. Biol. Chem. 266: 5980-5990.
14. Gentry DR, Cashel M. 1996. Mutational analysis of the Escherichia coli spoT gene identifies distinct but overlapping regions involved in ppGpp synthesis and degradation. Mol. Microbiol. 19:1373-1384.
15. Mechold U, Cashel M, Steiner K, Gentry D, Malke H. 1996. Functional analysis of a relA/spoT gene homolog from Streptococcus equisimilis. J. Bacteriol. 178:1401-1411.
16. Mechold U, Murphy H, Brown L, Cashel M. 2002. Intramolecular regulation of the opposing (p)ppGpp catalytic activities of Rel(Seq), the Rel/Spo enzyme from Streptococcus equisimilis. J. Bacteriol. 184: 2878-2888.
17. Abranches J, Martinez AR, Kajfasz JK, Chávez V, Garsin DA, Lemos JA. 2009. The molecular alarmone (p)ppGpp mediates stress responses, vancomycin tolerance, and virulence in Enterococcus faecalis. J. Bacteriol. 191: 2248-2256.
18. Lemos JA, Lin VK, Nascimento MM, Abranches J, Burne RA. 2007. Three gene products govern (p)ppGpp production by Streptococcus mutans. Mol. Microbiol. 65:1568-1581.
19. Nanamiya H, Kasai K, Nozawa A, Yun CS, Narisawa T, Murakami K, Natori Y, Kawamura F, Tozawa Y. 2008. Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis. Mol. Microbiol. 67:291-304.
20. Battesti A, Bouveret E. 2006. Acyl carrier protein/SpoT interaction, the switch linking SpoT-dependent stress response to fatty acid metabolism. Mol. Microbiol. 62:1048-1063.
21. Yan X, Zhao C, Budin-Verneuil A, Hartke A, Rincé A, Gilmore MS, Auffray Y, Pichereau V. 2009. The (p)ppGpp synthetase RelA contributes to stress adaptation and virulence in Enterococcus faecalis V583. Microbiology 155:3226-3237.
22. Ryals J, Little R, Bremer H. 1982. Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate. J. Bacteriol. 151: 1261-1268.
23. Sarubbi E, Rudd KE, Cashel M. 1988. Basal ppGpp level adjustment shown by new spoT mutants affect steady state growth rates and rrnA ribosomal promoter regulation in Escherichia coli. Mol. Gen. Genet. 213: 214-222.
24. Lazzarini RA, Cashel M, Gallant J. 1971. On the regulation of guanosine tetraphosphate levels in stringent and relaxed strains of Escherichia coli. J. Biol. Chem. 246:4381-4385.
25. Sokawa Y, Sokawa J, Kaziro Y. 1975. Regulation of stable RNA synthesis and ppGpp levels in growing cells of Escherichia coli. Cell 5:69-74.
26. Cashel M, Gentry D, Hernandez VJ, Vinella D. 1996. The stringent response, p 1458-1496. In Neidhardt FC, Ingraham JL, Low BK, Magasanik B, Schaechter M, Umbarger HE (ed), Escherichia coli and Salmonella typhimurium: cellular and molecular biology, 2nd ed. ASM Press, Washington, DC.
27. Dalebroux ZD, Yagi BF, Sahr T, Buchrieser C, Swanson MS. 2010. Distinct roles of ppGpp and DksA in Legionella pneumophila differentiation. Mol. Microbiol. 76:200-219.
28. Amato SM, Orman MA, Brynildsen MP. 2013. Metabolic control of persister formation in Escherichia coli. Mol. Cell 50:475-487.
29. Gerdes K, Maisonneuve E. 2012. Bacterial persistence and toxinantitoxin loci. Annu. Rev. Microbiol. 66:103-123.
30. Paulsen IT, Banerjei L, Myers GS, Nelson KE, Seshadri R, Read TD, Fouts DE, Eisen JA, Gill SR, Heidelberg JF, Tettelin H, Dodson RJ, Umayam L, Brinkac L, Beanan M, Daugherty S, DeBoy RT, Durkin S, Kolonay J, Madupu R, Nelson W, Vamathevan J, Tran B, Upton J, Hansen T, Shetty J, Khouri H, Utterback T, Radune D, Ketchum KA, Dougherty BA, Fraser CM. 2003. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299:2071-2074.
31. Bourgogne A, Garsin DA, Qin X, Singh KV, Sillanpaa J, Yerrapragada S, Ding Y, Dugan-Rocha S, Buhay C, Shen H, Chen G, Williams G, Muzny D, Maadani A, Fox KA, Gioia J, Chen L, Shang Y, Arias CA, Nallapareddy SR, Zhao M, Prakash VP, Chowdhury S, Jiang H, Gibbs RA, Murray BE, Highlander SK, Weinstock GM. 2008. Large scale variation in Enterococcus faecalis illustrated by the genome analysis of strain OG1RF. Genome Biol. 9:R110.
32. Seidl K, Müller S, François P, Kriebitzsch C, Schrenzel J, Engelmann S, Bischoff M, Berger-Bächi B. 2009. Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol. 9:95.
33. Bizzini A, Zhao C, Budin-Verneuil A, Sauvageot N, Giard JC, Auffray Y, Hartke A. 2010. Glycerol is metabolized in a complex and straindependent manner in Enterococcus faecalis. J. Bacteriol. 192:779-785.
34. Thomas TD, Ellwood DC, Longyear VM. 1979. Change from homoto heterolactic fermentation by Streptococcus lactis resulting from glucose limitation in anaerobic chemostat cultures. J. Bacteriol. 138:109-117.
35. Nyström T, Larsson C, Gustafsson L. 1996. Bacterial defense against aging: role of the Escherichia coli ArcA regulator in gene expression, readjusted energy flux and survival during stasis. EMBO J. 15:3219-3228.
36. Pugh SY, Knowles CJ. 1982. Growth of Streptococcus faecalis var. zymogenes on glycerol: the effect of aerobic and anaerobic growth in the presence and absence of haematin on enzyme synthesis. J. Gen. Microbiol. 128:1009-1017.
37. Huycke MM, Moore D, Joyce W, Wise P, Shepard L, Kotake Y, Gilmore MS. 2001. Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol. Microbiol. 42:729-740.
38. Fridovich I. 1983. Superoxide radical: an endogenous toxicant. Annu. Rev. Pharmacol. Toxicol. 23:239-257.
39. Rodionov DG, Ishiguro EE. 1995. Direct correlation between overproduction of guanosine 3=,5=-bispyrophosphate (ppGpp) and penicillin tolerance in Escherichia coli. J. Bacteriol. 177:4224-4229.
40. Kusser W, Ishiguro EE. 1987. Suppression of mutations conferring penicillin tolerance by interference with the stringent control mechanism of Escherichia coli. J. Bacteriol. 169:4396-4398.
41. Khakimova M, Ahlgren HG, Harrison JJ, English AM, Nguyen D. 2013. The stringent response controls catalases in Pseudomonas aeruginosa and is required for hydrogen peroxide and antibiotic tolerance. J. Bacteriol. 195:2011-2020.
42. Natori Y, Tagami K, Murakami K, Yoshida S, Tanigawa O, Moh Y, Masuda K, Wada T, Suzuki S, Nanamiya H, Tozawa Y, Kawamura F. 2009. Transcription activity of individual rrn operons in Bacillus subtilis mutants deficient in (p)ppGpp synthetase genes, relA, yjbM, and ywaC. J. Bacteriol. 191:4555-4561.
43. Srivatsan A, Han Y, Peng J, Tehranchi AK, Gibbs R, Wang JD, Chen R. 2008. High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet. 4:e1000139. doi:10.1371/ journal.pgen.1000139.
44. Mechold U, Potrykus K, Murphy H, Murakami KS, Cashel M. 2013. Differential regulation by ppGpp versus pppGpp in Escherichia coli. Nucleic Acids Res. 41:6175-6189.
45. Choi MY, Wang Y, Wong LL, Lu BT, Chen WY, Huang JD, Tanner JA, Watt RM. 2012. The two PPX-GppA homologues from Mycobacterium tuberculosis have distinct biochemical activities. PLoS One 7:e42561.
46. Somerville CR, Ahmed A. 1979. Mutants of Escherichia coli defective in the degradation of guanosine 5=-triphosphate, 3=-diphosphate (pppGpp). Mol. Gen. Genet. 169:315-323.
47. Keasling JD, Bertsch L, Kornberg A. 1993. Guanosine pentaphosphate phosphohydrolase of Escherichia coli is a long-chain exopolyphosphatase. Proc. Natl. Acad. Sci. U. S. A. 90:7029-7033.
48. Hamel E, Cashel M. 1973. Role of guanine nucleotides in protein synthesis. Elongation factors G and guanosine 5'-triphosphate,3'-diphosphate. Proc. Nat. Acad. Sci, U. S. A. 70:3250-3254.
49. Suárez CA, Blancato VS, Poncet S, Deutscher J, Magni C. 2011. CcpA represses the expression of the divergent cit operons of Enterococcus faecalis through multiple cre sites. BMC Microbiol. 11:227.
50. Darbon E, Servant P, Poncet S, Deutscher J. 2002. Antitermination by GlpP, catabolite repression via CcpA and inducer exclusion triggered by P-GlpK dephosphorylation control Bacillus subtilis glpFK expression. Mol. Microbiol. 43:1039-1052.
51. Abranches J, Nascimento MM, Zeng L, Browngardt CM, Wen ZT, Rivera MF, Burne RA. 2008. CcpA regulates central metabolism and virulence gene expression in Streptococcus mutans. J. Bacteriol. 190: 2340-2349.
52. Deutscher J, Küster E, Bergstedt U, Charrier V, Hillen W. 1995. Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in gram-positive bacteria. Mol. Microbiol. 15: 1049-1053.
53. Keren I, Wu Y, Inocencio J, Mulcahy LR, Lewis K. 2013. Killing by bactericidal antibiotics does not depend on reactive oxygen species. Science 339:1213-1216.
54. Liu Y, Imlay JA. 2013. Cell death from antibiotics without the involvement of reactive oxygen species. Science 339:1210-1213.
55. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ. 2007. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797-810.
56. Cashel M. 1975. Regulation of bacterial ppGpp and pppGpp. Annu. Rev. Microbiol. 29:301-318.
57. Sonenshein AL. 2007. Control of key metabolic intersections in Bacillus subtilis. Nat. Rev. Microbiol. 5:917-927.
58. Pall ML. 1985. GTP: a central regulator of cellular anabolism. Curr. Top. Cell. Regul. 25:1-20.
59. Nguyen D, Joshi-Datar A, Lepine F, Bauerle E, Olakanmi O, Beer K, McKay G, Siehnel R, Schafhauser J, Wang Y, Britigan BE, Singh PK. 2011. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334:982-986.
60. Bokinsky G, Baidoo EE, Akella S, Burd H, Weaver D, Alonso-Gutierrez J, García-Martín H, Lee TS, Keasling JD. 2013. HipA-Triggered growth arrest and beta-lactam tolerance in Escherichia coli are mediated by RelAdependent ppGpp synthesis. J. Bacteriol. 195:3173-3182.
61. Gao W, Chua K, Davies JK, Newton HJ, Seemann T, Harrison PF, Holmes NE, Rhee HW, Hong JI, Hartland EL, Stinear TP, Howden BP. 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:e1000944. doi:10.1371/ journal.ppat.1000944.
62. Mwangi MM, Kim C, Chung M, Tsai J, Vijayadamodar G, Benitez M, Jarvie TP, Du L, Tomasz A. 2013. Whole-genome sequencing reveals a link between beta-lactam resistance and synthetases of the alarmone (p)ppGpp in Staphylococcus aureus. Microb. Drug Resist. 19:153-159.
63. Terleckyj B, Willett NP, Shockman GD. 1975. Growth of several cariogenic strains of oral streptococci in a chemically defined medium. Infect. Immun. 11:649-655.
64. Abranches J, Candella MM, Wen ZT, Baker HV, Burne RA. 2006. Different roles of EIIABMan and EIIGlc in regulation of energy metabolism, biofilm development, and competence in Streptococcus mutans. J. Bacteriol. 188:3748-3756.
65. Zhu A, Romero R, Petty HR. 2010. Amplex UltraRed enhances the sensitivity of fluorimetric pyruvate detection. Anal. Biochem. 403: 123-125.
66. Repizo GD, Mortera P, Magni C. 2011. Disruption of the alsSD operon of Enterococcus faecalis impairs growth on pyruvate at low pH. Microbiology 157:2708-2719.
67. Stols L, Gu M, Dieckman L, Raffen R, Collart FR, Donnelly MI. 2002. A new vector for high-throughput, ligation-independent cloning encoding a tobacco etch virus protease cleavage site. Protein Expr. Purif. 25: 8-15.