Environmental salinity determines the specificity and need for tat-dependent secretion of the YwbN protein in Bacillus subtilis

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  van der Ploeg, René ^a   Mäder, Ulrike ^b   Homuth, Georg ^b   Schaffer, Marc ^b   Denham, Emma L ^a   Monteferrante, Carmine G ^a   Miethke, Marcus ^c   Marahiel, Mohamed A ^c   Harwood, Colin R ^d   Winter, Theresa ^b   Hecker, Michael ^b   Antelmann, Haike ^b   van Dijl, Jan Maarten ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GREIFSWALD   (Germany)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; IRON; PEROXIDASE; PROTEIN TATAD; PROTEIN TATAY; PROTEIN TATCY; PROTEIN YWBN; SODIUM CHLORIDE; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM MUTANT; CONTROLLED STUDY; CULTURE MEDIUM; CYTOLYSIS; ENVIRONMENTAL STRESS; GROWTH RATE; IRON TRANSPORT; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SECRETION; SALINITY; SALT TOLERANCE; ENVIRONMENT; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NORTHERN BLOTTING; PHENOTYPE; PLASMID; SECRETION;

ARCHAEA; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); POSIBACTERIA;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BLOTTING, NORTHERN; ENVIRONMENT; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; IRON; MEMBRANE TRANSPORT PROTEINS; PHENOTYPE; PLASMIDS; SALINITY; TRANSCRIPTION, GENETIC;

EID: 79953317279     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018140     Document Type: Article

References (57)

1. Robinson C, Bolhuis A, (2004) Tat-dependent protein targeting in prokaryotes and chloroplasts. Biochim Biophys Acta 1694: 135-147.
2. Palmer T, Sargent F, Berks BC, (2005) Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol 13: 175-180.
3. Driessen AJ, Nouwen N, (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77: 643-667.
4. Natale P, Bruser T, Driessen AJ, (2008) Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane-distinct translocases and mechanisms. Biochim Biophys Acta 1778: 1735-1756.
5. Sargent F, (2007) The twin-arginine transport system: moving folded proteins across membranes. Biochem Soc Trans 35: 835-847.
6. Berks BC, Sargent F, Palmer T, (2000) The Tat protein export pathway. Mol Microbiol 35: 260-274.
7. DeLisa MP, Tullman D, Georgiou G, (2003) Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc Natl Acad Sci U S A 100: 6115-6120.
8. Panahandeh S, Maurer C, Moser M, Delisa MP, Muller M, (2008) Following the path of a twin-arginine precursor along the TatABC translocase of Escherichia coli. J Biol Chem 283: 33267-33275.
9. Wexler M, Bogsch EG, Klosgen RB, Palmer T, Robinson C, et al. (1998) Targeting signals for a bacterial Sec-independent export system direct plant thylakoid import by the delta pH pathway. FEBS Lett 431: 339-342.
10. Berks BC, (1996) A common export pathway for proteins binding complex redox cofactors? Mol Microbiol 22: 393-404.
11. Chaddock AM, Mant A, Karnauchov I, Brink S, Herrmann RG, et al. (1995) A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the delta pH-dependent thylakoidal protein translocase. Embo J 14: 2715-2722.
12. Brink S, Bogsch EG, Edwards WR, Hynds PJ, Robinson C, (1998) Targeting of thylakoid proteins by the delta pH-driven twin-arginine translocation pathway requires a specific signal in the hydrophobic domain in conjunction with the twin-arginine motif. FEBS Lett 434: 425-430.
13. 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.
14. Cristobal S, de Gier JW, Nielsen H, von Heijne G, (1999) Competition between Sec- and TAT-dependent protein translocation in Escherichia coli. Embo J 18: 2982-2990.
15. DeLisa MP, Samuelson P, Palmer T, Georgiou G, (2002) Genetic analysis of the twin arginine translocator secretion pathway in bacteria. J Biol Chem 277: 29825-29831.
16. Sargent F, Bogsch EG, Stanley NR, Wexler M, Robinson C, et al. (1998) Overlapping functions of components of a bacterial Sec-independent protein export pathway. Embo J 17: 3640-3650.
17. Bogsch EG, Sargent F, Stanley NR, Berks BC, Robinson C, et al. (1998) An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J Biol Chem 273: 18003-18006.
18. Jongbloed JD, Martin U, Antelmann H, Hecker M, Tjalsma H, et al. (2000) TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J Biol Chem 275: 41350-41357.
19. Jongbloed JD, Antelmann H, Hecker M, Nijland R, Bron S, et al. (2002) Selective contribution of the twin-arginine translocation pathway to protein secretion in Bacillus subtilis. J Biol Chem 277: 44068-44078.
20. Jongbloed JD, Grieger U, Antelmann H, Hecker M, Nijland R, et al. (2004) Two minimal Tat translocases in Bacillus. Mol Microbiol 54: 1319-1325.
21. Jongbloed JD, van der Ploeg R, van Dijl JM, (2006) Bifunctional TatA subunits in minimal Tat protein translocases. Trends Microbiol 14: 2-4.
22. Bolhuis A, Mathers JE, Thomas JD, Barrett CM, Robinson C, (2001) TatB and TatC form a functional and structural unit of the twin-arginine translocase from Escherichia coli. J Biol Chem 276: 20213-20219.
23. Cline K, Mori H, (2001) Thylakoid DeltapH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J Cell Biol 154: 719-729.
24. Alami M, Luke I, Deitermann S, Eisner G, Koch HG, et al. (2003) Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol Cell 12: 937-946.
25. Mori H, Cline K, (2002) A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid [Delta]pH/Tat translocase. J Cell Biol 157: 205-210.
26. Yen MR, Tseng YH, Nguyen EH, Wu LF, Saier MH Jr, (2002) Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch Microbiol 177: 441-450.
27. Sturm A, Schierhorn A, Lindenstrauss U, Lilie H, Bruser T, (2006) YcdB from Escherichia coli reveals a novel class of Tat-dependently translocated hemoproteins. J Biol Chem 281: 13972-13978.
28. Widdick DA, Eijlander RT, van Dijl JM, Kuipers OP, Palmer T, (2007) A Facile Reporter System for the Experimental Identification of Twin-Arginine Translocation (Tat) Signal Peptides from All Kingdoms of Life. J Mol Biol.
29. Kouwen TR, van der Ploeg R, Antelmann H, Hecker M, Homuth G, et al. (2009) Overflow of a hyper-produced secretory protein from the Bacillus Sec pathway into the Tat pathway for protein secretion as revealed by proteogenomics. Proteomics.
30. Rose RW, Bruser T, Kissinger JC, Pohlschroder 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.
31. Bolhuis A, (2002) Protein transport in the halophilic archaeon Halobacterium sp. NRC-1: a major role for the twin-arginine translocation pathway? Microbiology 148: 3335-3346.
32. Thomas JR, Bolhuis A, (2006) The tatC gene cluster is essential for viability in halophilic archaea. FEMS Microbiol Lett 256: 44-49.
33. Hutcheon GW, Bolhuis A, (2003) The archaeal twin-arginine translocation pathway. Biochem Soc Trans 31: 686-689.
34. Dilks K, Gimenez MI, Pohlschroder M, (2005) Genetic and biochemical analysis of the twin-arginine translocation pathway in halophilic archaea. J Bacteriol 187: 8104-8113.
35. Gimenez MI, Dilks K, Pohlschroder M, (2007) Haloferax volcanii twin-arginine translocation substates include secreted soluble, C-terminally anchored and lipoproteins. Mol Microbiol 66: 1597-1606.
36. Eijlander RT, Jongbloed JD, Kuipers OP, (2009) Relaxed specificity of the Bacillus subtilis TatAdCd translocase in Tat-dependent protein secretion. J Bacteriol 191: 196-202.
37. Rasmussen S, Nielsen HB, Jarmer H, (2009) The transcriptionally active regions in the genome of Bacillus subtilis. Mol Microbiol 73: 1043-1057.
38. Cao J, Woodhall MR, Alvarez J, Cartron ML, Andrews SC, (2007) EfeUOB (YcdNOB) is a tripartite, acid-induced and CpxAR-regulated, low-pH Fe2+ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7. Mol Microbiol 65: 857-875.
39. Biswas L, Biswas R, Nerz C, Ohlsen K, Schlag M, et al. (2009) Role of the twin-arginine translocation pathway in Staphylococcus. J Bacteriol 191: 5921-5929.
40. May JJ, Wendrich TM, Marahiel MA, (2001) The dhb operon of Bacillus subtilis encodes the biosynthetic template for the catecholic siderophore 2,3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J Biol Chem 276: 7209-7217.
41. Hantke K, (1997) Ferrous iron uptake by a magnesium transport system is toxic for Escherichia coli and Salmonella typhimurium. J Bacteriol 179: 6201-6204.
42. Moore CM, Helmann JD, (2005) Metal ion homeostasis in Bacillus subtilis. Curr Opin Microbiol 8: 188-195.
43. Ollinger J, Song KB, Antelmann H, Hecker M, Helmann JD, (2006) Role of the Fur regulon in iron transport in Bacillus subtilis. J Bacteriol 188: 3664-3673.
44. Kolkman MA, van der Ploeg R, Bertels M, van Dijk M, van der Laan J, et al. (2008) The twin-arginine signal peptide of Bacillus subtilis YwbN can direct either Tat- or Sec-dependent secretion of different cargo proteins: secretion of active subtilisin via the B. subtilis Tat pathway. Appl Environ Microbiol 74: 7507-7513.
45. Hoper D, Bernhardt J, Hecker M, (2006) Salt stress adaptation of Bacillus subtilis: a physiological proteomics approach. Proteomics 6: 1550-1562.
46. Bursy J, Pierik AJ, Pica N, Bremer E, (2007) Osmotically induced synthesis of the compatible solute hydroxyectoine is mediated by an evolutionarily conserved ectoine hydroxylase. J Biol Chem 282: 31147-31155.
47. Grosse C, Scherer J, Koch D, Otto M, Taudte N, et al. (2006) A new ferrous iron-uptake transporter, EfeU (YcdN), from Escherichia coli. Mol Microbiol 62: 120-131.
48. Kosman DJ, (2003) Molecular mechanisms of iron uptake in fungi. Mol Microbiol 47: 1185-1197.
49. Askwith C, Kaplan J, (1997) An oxidase-permease-based iron transport system in Schizosaccharomyces pombe and its expression in Saccharomyces cerevisiae. J Biol Chem 272: 401-405.
50. Letoffe S, Heuck G, Delepelaire P, Lange N, Wandersman C, (2009) Bacteria capture iron from heme by keeping tetrapyrrol skeleton intact. Proc Natl Acad Sci U S A 106: 11719-11724.
51. Hoffmann T, Schutz A, Brosius M, Volker A, Volker U, et al. (2002) High-salinity-induced iron limitation in Bacillus subtilis. J Bacteriol 184: 718-727.
52. Steil L, Hoffmann T, Budde I, Volker U, Bremer E, (2003) Genome-wide transcriptional profiling analysis of adaptation of Bacillus subtilis to high salinity. J Bacteriol 185: 6358-6370.
53. Miethke M, Klotz O, Linne U, May JJ, Beckering CL, et al. (2006) Ferri-bacillibactin uptake and hydrolysis in Bacillus subtilis. Mol Microbiol 61: 1413-1427.
54. Tjalsma H, Bolhuis A, van Roosmalen ML, Wiegert T, Schumann W, et al. (1998) Functional analysis of the secretory precursor processing machinery of Bacillus subtilis: identification of a eubacterial homolog of archaeal and eukaryotic signal peptidases. Genes Dev 12: 2318-2331.
55. Darmon E, Dorenbos R, Meens J, Freudl R, Antelmann H, et al. (2006) A disulfide bond-containing alkaline phosphatase triggers a BdbC-dependent secretion stress response in Bacillus subtilis. Appl Environ Microbiol 72: 6876-6885.
56. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, et al. (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390: 249-256.
57. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, et al. (2003) Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A 100: 4678-4683.