Twin-arginine translocation system in Helicobacter pylori: TatC, but Not TatB, essential for viability

mBio

Volumn 5, Issue 1, 2014, Pages

  Benoit, Stéphane L ^a   Maier, Robert J ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CATALASE; GLUTAMINASE; HYDROGENASE; ISOPROPYL THIOGALACTOSIDE; TWIN ARGININE TRANSLOCATION A PROTEIN; TWIN ARGININE TRANSLOCATION B PROTEIN; TWIN ARGININE TRANSLOCATION C PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; HELICOBACTER PYLORI; HOMOLOGOUS RECOMBINATION; MICROSCOPY; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUEA GENE; STOMACH; TATA GENE; TATB GENE; TATC GENE; WILD TYPE;

ANIMALS; BACTERIAL PROTEINS; CATALASE; DISEASE MODELS, ANIMAL; GENE KNOCKOUT TECHNIQUES; GENES, ESSENTIAL; GENETIC COMPLEMENTATION TEST; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HYDROGENASE; MEMBRANE TRANSPORT PROTEINS; MICE; MICROBIAL VIABILITY; VIRULENCE;

EID: 84903370967     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01016-13     Document Type: Article

References (56)

1. Wickner W, Schekman R. 2005. Protein translocation across biological membranes. Science 310:1452-1456. http://dx.doi.org/10.1126/ science.1113752.
2. Berks BC, Palmer T, Sargent F. 2005. Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr. Opin. Microbiol. 8:174-181. http://dx.doi.org/10.1016/j.mib.2005.02.010.
3. Palmer T, Sargent F, Berks BC. 2005. Export of complex cofactorcontaining proteins by the bacterial Tat pathway. Trends Microbiol. 13: 175-180. http://dx.doi.org/10.1016/j.tim.2005.02.002.
4. Stanley NR, Palmer T, Berks BC. 2000. The twin arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli. J. Biol. Chem. 275:11591-11596. http://dx.doi.org/ 10.1074/jbc.275.16.11591.
5. Palmer T, Berks BC. 2012. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 10:483-496. http://dx.doi.org/ 10.1038/nrmicro2814.
6. Wexler M, Sargent F, Jack RL, Stanley NR, Bogsch EG, Robinson C, Berks BC, Palmer T. 2000. TatD is a cytoplasmic protein with DNase activity. No requirement for TatD family proteins in sec-independent protein export. J. Biol. Chem. 275:16717-16722. http://dx.doi.org/ 10.1074/jbc.M000800200.
7. Sargent F, Bogsch EG, Stanley NR, Wexler M, Robinson C, Berks BC, Palmer T. 1998. Overlapping functions of components of a bacterial Secindependent protein export pathway. EMBO J. 17:3640-3650. http:// dx.doi.org/10.1093/emboj/17.13.3640.
8. Lee PA, Orriss GL, Buchanan G, Greene NP, Bond PJ, Punginelli C, Jack RL, Sansom MS, Berks BC, Palmer T. 2006. Cysteine-scanning mutagenesis and disulfide mapping studies of the conserved domain of the twin-arginine translocase TatB component. J. Biol. Chem. 281: 34072-34085. http://dx.doi.org/10.1074/jbc.M607295200.
9. Mickael CS, Lam PK, Berberov EM, Allan B, Potter AA, Köster W. 2010. Salmonella enterica serovar Enteritidis tatB and tatC mutants are impaired in Caco-2 cell invasion in vitro and show reduced systemic spread in chickens. Infect. Immun. 78:3493-3505. http://dx.doi.org/ 10.1128/IAI.00090-10.
10. Lavander M, Ericsson SK, Bröms JE, Forsberg A. 2006. The twin arginine translocation system is essential for virulence of Yersinia pseudotuberculosis. Infect. Immun. 74:1768-1776. http://dx.doi.org/10.1128/ IAI.74.3.1768-1776.2006.
11. Zhang L, Zhu Z, Jing H, Zhang J, Xiong Y, Yan M, Gao S, Wu LF, Xu J, Kan B. 2009. Pleiotropic effects of the twin-arginine translocation system on biofilm formation, colonization, and virulence in Vibrio cholerae. BMC Microbiol. 9:114. http://dx.doi.org/10.1186/1471-2180-9-114.
12. Rodríguez-Sanz M, Antúnez-Lamas M, Rojas C, López-Solanilla E, Palacios JM, Rodríguez-Palenzuela P, Rey L. 2010. The Tat pathway of plant pathogen Dickeya dadantii 3937 contributes to virulence and fitness. FEMS Microbiol. Lett. 302:151-158. http://dx.doi.org/10.1111/j.1574-6968.2009.01844.x.
13. Rajashekara G, Drozd M, Gangaiah D, Jeon B, Liu Z, Zhang Q. 2009. Functional characterization of the twin-arginine translocation system in Campylobacter jejuni. Foodborne Pathog. Dis. 6:935-945. http:// dx.doi.org/10.1089/fpd.2009.0298.
14. Pickering BS, Oresnik IJ. 2010. The twin arginine transport system appears to be essential for viability in Sinorhizobium meliloti. J. Bacteriol. 192:5173-5180. http://dx.doi.org/10.1128/JB.00206-10.
15. Chang CY, Hobley L, Till R, Capeness M, Kanna M, Burtt W, Jagtap P, Aizawa S, Sockett RE. 2011. The Bdellovibrio bacteriovorus twin-arginine transport system has roles in predatory and prey-independent growth. Microbiology 157:3079-3093. http://dx.doi.org/10.1099/mic.0.052449-0.
16. Saint-Joanis B, Demangel C, Jackson M, Brodin P, Marsollier L, Boshoff H, Cole ST. 2006. Inactivation of Rv2525c, a substrate of the twin arginine translocation (Tat) system of Mycobacterium tuberculosis, increases beta-lactam susceptibility and virulence. J. Bacteriol. 188: 6669-6679. http://dx.doi.org/10.1128/JB.00631-06.
17. Dilks K, Giménez MI, Pohlschröder M. 2005. Genetic and biochemical analysis of the twin-arginine translocation pathway in halophilic archaea. J. Bacteriol. 187:8104-8113. http://dx.doi.org/10.1128/JB.187.23.8104-8113.2005.
18. Thomas JR, Bolhuis A. 2006. The tatC gene cluster is essential for viability in halophilic archaea. FEMS Microbiol. Lett. 256:44-49. http:// dx.doi.org/10.1111/j.1574-6968.2006.00107.x.
19. Marshall BJ, Warren JR. 1984. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1:1311-1315.
20. Covacci A, Telford JL, Del Giudice G, Parsonnet J, Rappuoli R. 1999. Helicobacter pylori virulence and genetic geography. Science 284: 1328-1333. http://dx.doi.org/10.1126/science.284.5418.1328.
21. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, Ketchum KA, Klenk HP, Gill S, Dougherty BA, Nelson K, Quackenbush J, Zhou L, Kirkness EF, Peterson S, Loftus B, Richardson D, Dodson R, Khalak HG, Glodek A, McKenney K, Fitzegerald LM, Lee N, Adams MD, Hickey EK, Berg DE, Gocayne JD, Utterback TR, Peterson JD, Kelley JM, Cotton MD, Weidman JM, Fujii C, Bowman C, Watthey L, Wallin E, Hayes WS, Borodovsky M, Karp PD, Smith HO, Fraser CM, Venter JC. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547. http:// dx.doi.org/10.1038/41483.
22. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, Sittka A, Chabas S, Reiche K, Hackermüller J, Reinhardt R, Stadler PF, Vogel J. 2010. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464:250-255. http://dx.doi.org/10.1038/ nature08756.
23. Sargent F, Stanley NR, Berks BC, Palmer T. 1999. Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J. Biol. Chem. 274:36073-36082.
24. Alm RA, Ling LS, Moir DT, King BL, Brown ED, Doig PC, Smith DR, Noonan B, Guild BC, deJonge BL, Carmel G, Tummino PJ, Caruso A, Uria-Nickelsen M, Mills DM, Ives C, Gibson R, Merberg D, Mills SD, Jiang Q, Taylor DE, Vovis GF, Trust TJ. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180. http://dx.doi.org/10.1038/16495.
25. Oh JD, Kling-Bäckhed H, Giannakis M, Xu J, Fulton RS, Fulton LA, Cordum HS, Wang C, Elliott G, Edwards J, Mardis ER, Engstrand LG, Gordon JI. 2006. The complete genome sequence of a chronic atrophic gastritis Helicobacter pylori strain: evolution during disease progression. Proc. Natl. Acad. Sci. U. S. A. 103:9999-10004. http://dx.doi.org/10.1073/ pnas.0603784103.
26. Baltrus DA, Amieva MR, Covacci A, Lowe TM, Merrell DS, Ottemann KM, Stein M, Salama NR, Guillemin K. 2009. The complete genome sequence of Helicobacter pylori strain G27. J. Bacteriol. 191:447-448. http://dx.doi.org/10.1128/JB.01416-08.
27. McClain MS, Shaffer CL, Israel DA, Peek RM, Jr, Cover TL. 2009. Genome sequence analysis of Helicobacter pylori strains associated with gastric ulceration and gastric cancer. BMC Genomics 10:3. http:// dx.doi.org/10.1186/1471-2164-10-S1-S3.
28. Robinson C, Matos CF, Beck D, Ren C, Lawrence J, Vasisht N, Mendel S. 2011. Transport and proofreading of proteins by the twin-arginine translocation (Tat) system in bacteria. Biochim. Biophys. Acta 1808: 876-884. http://dx.doi.org/10.1016/j.bbamem.2010.11.023.
29. Bagos PG, Nikolaou EP, Liakopoulos TD, Tsirigos KD. 2010. Combined prediction of Tat and Sec signal peptides with hidden Markov models. Bioinformatics 26:2811-2817. http://dx.doi.org/10.1093/bioinformatics/ btq530.
30. Rose RW, Brüser T, Kissinger JC, Pohlschröder M. 2002. Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol. Microbiol. 45:943-950. http:// dx.doi.org/10.1046/j.1365-2958.2002.03090.x.
31. Bendtsen JD, Nielsen H, Widdick D, Palmer T, Brunak S. 2005. Prediction of twin-arginine signal peptides. BMC Bioinformatics 6:167. http://dx.doi.org/10.1186/1471-2105-6-167.
32. Gorrell RJ, Yang J, Kusters JG, van Vliet AH, Robins-Browne RM. 2005. Restriction of DNA encoding selectable markers decreases the transformation efficiency of Helicobacter pylori. FEMS Immunol. Med. Microbiol. 44:213-219. http://dx.doi.org/10.1016/j.femsim.2004.10.019.
33. Maier RJ, Fu C, Gilbert J, Moshiri F, Olson J, Plaut AG. 1996. Hydrogen uptake hydrogenase in Helicobacter pylori. FEMS Microbiol. Lett. 141: 71-76. http://dx.doi.org/10.1111/j.1574-6968.1996.tb08365.x.
34. Harris AG, Hazell SL. 2003. Localisation of Helicobacter pylori catalase in both the periplasm and cytoplasm, and its dependence on the twinarginine target protein, KapA, for activity. FEMS Microbiol. Lett. 229: 283-289. http://dx.doi.org/10.1016/S0378-1097(03)00850-4.
35. Rain JC, Selig L, De Reuse H, Battaglia V, Reverdy C, Simon S, Lenzen G, Petel F, Wojcik J, Schächter V, Chemama Y, Labigne A, Legrain P. 2001. The protein-protein interaction map of Helicobacter pylori. Nature 409:211-215. http://dx.doi.org/10.1038/35051615.
36. Chevalier C, Thiberge JM, Ferrero RL, Labigne A. 1999. Essential role of Helicobacter pylori gamma-glutamyltranspeptidase for the colonization of the gastric mucosa of mice. Mol. Microbiol. 31:1359-1372. http:// dx.doi.org/10.1046/j.1365-2958.1999.01271.x.
37. Valenzuela M, Bravo D, Canales J, Sanhueza C, Díaz N, Almarza O, Toledo H, Quest AF. 2013. Helicobacter pylori-induced loss of survivin and gastric cell viability is attributable to secreted bacterial gammaglutamyl transpeptidase activity. J. Infect. Dis. 208:1131-1141. http:// dx.doi.org/10.1093/infdis/jit286.
38. Harris AG, Wilson JE, Danon SJ, Dixon MF, Donegan K, Hazell SL. 2003. Catalase (KatA) and KatA-associated protein (KapA) are essential to persistent colonization in the Helicobacter pylori SS1 mouse model. Microbiology 149:665-672. http://dx.doi.org/10.1099/mic.0.26012-0.
39. Olson JW, Maier RJ. 2002. Molecular hydrogen as an energy source for Helicobacter pylori. Science 298:1788-1790. http://dx.doi.org/10.1126/ science.1077123.
40. Boneca IG, Ecobichon C, Chaput C, Mathieu A, Guadagnini S, Prévost MC, Colland F, Labigne A, de Reuse H. 2008. Development of inducible systems to engineer conditional mutants of essential genes of Helicobacter pylori. Appl. Environ. Microbiol. 74:2095-2102. http://dx.doi.org/ 10.1128/AEM.01348-07.
41. Salama NR, Shepherd B, Falkow S. 2004. Global transposon mutagenesis and essential gene analysis of Helicobacter pylori. J. Bacteriol. 186: 7926-7935. http://dx.doi.org/10.1128/JB.186.23.7926-7935.2004.
42. Dilks K, Rose RW, Hartmann E, Pohlschröder M. 2003. Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J. Bacteriol. 185:1478-1483. http://dx.doi.org/10.1128/JB.185.4.1478-1483.2003.
43. Rodrigue A, Chanal A, Beck K, Müller M, Wu LF. 1999. Cotranslocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial tat pathway. J. Biol. Chem. 274:13223-13228. http://dx.doi.org/10.1074/jbc.274.19.13223.
44. Aldridge C, Spence E, Kirkilionis MA, Frigerio L, Robinson C. 2008. Tat-dependent targeting of Rieske iron-sulphur proteins to both the plasma and thylakoid membranes in the cyanobacterium Synechocystis PCC6803. Mol. Microbiol. 70:140-150. http://dx.doi.org/10.1111/j.1365-2958.2008.06401.x.
45. Bachmann J, Bauer B, Zwicker K, Ludwig B, Anderka O. 2006. The Rieske protein from Paracoccus denitrificans is inserted into the cytoplasmic membrane by the twin-arginine translocase. FEBS J 273:4817-4830. http://dx.doi.org/10.1111/j.1742-4658.2006.05480.x.
46. De Buck E, Vranckx L, Meyen E, Maes L, Vandersmissen L, Anné J, Lammertyn E. 2007. The twin-arginine translocation pathway is necessary for correct membrane insertion of the Rieske Fe/S protein in Legionella pneumophila. FEBS Lett. 581:259-264. http://dx.doi.org/10.1016/ j.febslet.2006.12.022.
47. Hopkins A, Buchanan G, Palmer T. 2013. The role of the twin arginine protein transport pathway in the assembly of the Streptomyces coelicolor A3(2) cytochrome bc1 complex. J. Bacteriol. 196:50-59.
48. Luo Q, Dong Y, Chen H, Gao H. 2013. Mislocalization of Rieske protein PetA predominantly accounts for the aerobic growth defect of Tat mutants in Shewanella oneidensis. PLoS One 8:e62064. http://dx.doi.org/ 10.1371/journal.pone.0062064.
49. Kelly DJ. 1998. The physiology and metabolism of the human gastric pathogen Helicobacter pylori. Adv. Microb. Physiol. 40:137-189. http:// dx.doi.org/10.1016/S0065-2911(08)60131-9.
50. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, Basham D, Chillingworth T, Davies RM, Feltwell T, Holroyd S, Jagels K, Karlyshev AV, Moule S, Pallen MJ, Penn CW, Quail MA, Rajandream MA, Rutherford KM, van Vliet AH, Whitehead S, Barrell BG. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665-668. http://dx.doi.org/ 10.1038/35001088.
51. Ize B, Stanley NR, Buchanan G, Palmer T. 2003. Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol. Microbiol. 48: 1183-1193. http://dx.doi.org/10.1046/j.1365-2958.2003.03504.x.
52. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786. http://dx.doi.org/10.1038/nmeth.1701.
53. Benoit S, Maier RJ. 2003. Dependence of Helicobacter pylori urease activity on the nickel-sequestering ability of the UreE accessory protein. J. Bacteriol. 185:4787-4795. http://dx.doi.org/10.1128/JB.185.16.4787-4795.2003.
54. Olson JW, Agar JN, Johnson MK, Maier RJ. 2000. Characterization of the NifU and NifS Fe-S cluster formation proteins essential for viability in Helicobacter pylori. Biochemistry 39:16213-16219. http://dx.doi.org/ 10.1021/bi001744s.
55. Stark RM, Suleiman MS, Hassan IJ, Greenman J, Millar MR. 1997. Amino acid utilisation and deamination of glutamine and asparagine by Helicobacter pylori. J. Med. Microbiol. 46:793-800. http://dx.doi.org/ 10.1099/00222615-46-9-793.
56. Weatherburn MW. 1967. Phenol-hypochlorite reaction for determination of ammonia. Anal. Chem. 39:971-974. http://dx.doi.org/10.1021/ ac60252a045.