The Bdellovibrio bacteriovorus twin-arginine transport system has roles in predatory and prey-independent growth

Microbiology

Volumn 157, Issue 11, 2011, Pages 3079-3093

  Chang, Chien Yi ^a   Hobley, Laura ^a   Till, Rob ^a   Capeness, Michael ^a   Kanna, Machi ^b   Burtt, William ^a   Jagtap, Pratik ^c   Aizawa, Shin Ichi ^b   Elizabeth Sockett, R ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b PREFECTURAL UNIVERSITY OF HIROSHIMA   (Japan)

^c MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; TWIN ARGININE TRANSLOCATION A1 PROTEIN; TWIN ARGININE TRANSLOCATION A2 PROTEIN; TWIN ARGININE TRANSLOCATION BC PROTEIN; TWIN ARGININE TRANSLOCATION C PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL MUTATION; BDELLOVIBRIO; BDELLOVIBRIO BACTERIOVORUS; CONTROLLED STUDY; ESCHERICHIA COLI; GENE INACTIVATION; GENE INSERTION; MUTAGENESIS; NONHUMAN; PREDATOR PREY INTERACTION; PRIORITY JOURNAL; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BDELLOVIBRIO; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PERIPLASM; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); BDELLOVIBRIO BACTERIOVORUS; ESCHERICHIA COLI; NEGIBACTERIA;

EID: 80155164952     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.052449-0     Document Type: Article

References (74)

1. Alami, M., Lüke, I., Deitermann, S., Eisner, G., Koch, H. G., Brunner, J. & Müller, M. (2003). Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol Cell 12, 937-946.
2. Amann, E., Ochs, B. & Abel, K. J. (1988). Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69, 301-315.
3. Bagos, P. G., Nikolaou, E. P., Liakopoulos, T. D. & Tsirigos, K. D. (2010). Combined prediction of Tat and Sec signal peptides with hidden Markov models. Bioinformatics 26, 2811-2817.
4. Barabote, R. D., Rendulic, S., Schuster, S. C. & Saier, M. H., Jr (2007). Comprehensive analysis of transport proteins encoded within the genome of Bdellovibrio bacteriovorus. Genomics 90, 424-446.
5. Barel, G. & Jurkevitch, E. (2001). Analysis of phenotypic diversity among host-independent mutants of Bdellovibrio bacteriovorus 109J. Arch Microbiol 176, 211-216.
6. Beloin, C., Valle, J., Latour-Lambert, P., Faure, P., Kzreminski, M., Balestrino, D., Haagensen, J. A., Molin, S., Prensier, G. & other authors (2004). Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51, 659-674.
7. Bendtsen, J. D., Nielsen, H., Widdick, D., Palmer, T. & Brunak, S. (2005). Prediction of twin-arginine signal peptides. BMC Bioinformatics 6, 167.
8. Berks, B. C. (1996). A common export pathway for proteins binding complex redox cofactors? Mol Microbiol 22, 393-404.
9. Berks, B. C., Palmer, T. & Sargent, F. (2005). Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr Opin Microbiol 8, 174-181.
10. Bernhardt, T. G. & de Boer, P. A. (2003). The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twinarginine transport pathway. Mol Microbiol 48, 1171-1182.
11. Bierman, M., Logan, R., O'Brien, K., Seno, E. T., Rao, R. N. & Schoner, B. E. (1992). Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116, 43-49.
12. Blaudeck, N., Kreutzenbeck, P., Müller, M., Sprenger, G. A. & Freudl, R. (2005). Isolation and characterization of bifunctional Escherichia coli TatA mutant proteins that allow efficient Tat-dependent protein translocation in the absence of TatB. J Biol Chem 280, 3426-3432.
13. Bogsch, E. G., Sargent, F., Stanley, N. R., Berks, B. C., Robinson, C. & Palmer, T. (1998). An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J Biol Chem 273, 18003-18006.
14. Bolhuis, A., Mathers, J. E., Thomas, J. D., Barrett, C. M. & 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.
15. Brüser, T. (2007). The twin-arginine translocation system and its capability for protein secretion in biotechnological protein production. Appl Microbiol Biotechnol 76, 35-45.
16. Buchanan, G., de Leeuw, E., Stanley, N. R., Wexler, M., Berks, B. C., Sargent, F. & Palmer, T. (2002). Functional complexity of the twinarginine translocase TatC component revealed by site-directed mutagenesis. Mol Microbiol 43, 1457-1470.
17. Casadaban, M. J. & Cohen, S. N. (1979). Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci U S A 76, 4530-4533.
18. Dabney-Smith, C., Mori, H. & Cline, K. (2006). Oligomers of Tha4 organize at the thylakoid Tat translocase during protein transport. J Biol Chem 281, 5476-5483.
19. De Buck, E., Lammertyn, E. & Anné, J. (2008). The importance of the twin-arginine translocation pathway for bacterial virulence. Trends Microbiol 16, 442-453.
20. DeLisa, M. P., Samuelson, P., Palmer, T. & Georgiou, G. (2002). Genetic analysis of the twin arginine translocator secretion pathway in bacteria. J Biol Chem 277, 29825-29831.
21. Dilks, K., Giménez, M. I. & Pohlschröder, M. (2005). Genetic and biochemical analysis of the twin-arginine translocation pathway in halophilic archaea. J Bacteriol 187, 8104-8113.
22. Dubini, A., Pye, R. L., Jack, R. L., Palmer, T. & Sargent, F. (2002). How bacteria get energy from hydrogen: a genetic analysis of periplasmic hydrogen oxidation in Escherichia coli. Int J Hydrogen Energy 27, 1413-1420.
23. Evans, K. J., Lambert, C. & Sockett, R. E. (2007). Predation by Bdellovibrio bacteriovorus HD100 requires type IV pili. J Bacteriol 189, 4850-4859.
24. Fenton, A. K., Kanna, M., Woods, R. D., Aizawa, S. I. & Sockett, R. E. (2010). Shadowing the actions of a predator: backlit fluorescent microscopy reveals synchronous nonbinary septation of predatory Bdellovibrio inside prey and exit through discrete bdelloplast pores. J Bacteriol 192, 6329-6335.
25. Gohlke, U., Pullan, L., McDevitt, C. A., Porcelli, I., de Leeuw, E., Palmer, T., Saibil, H. R. & Berks, B. C. (2005). The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc Natl Acad Sci U S A 102, 10482-10486.
26. González, A., Benini, S. & Ciurli, S. (2003). Structure of Rhodoferax fermentans high-potential iron-sulfur protein solved by MAD. Acta Crystallogr D Biol Crystallogr 59, 1582-1588.
27. Heikkilä, M. P., Honisch, U., Wunsch, P. & Zumft, W. G. (2001). Role of the Tat transport system in nitrous oxide reductase translocation and cytochrome cd1 biosynthesis in Pseudomonas stutzeri. J Bacteriol 183, 1663-1671.
28. Hobley, L., King, J. R. & Sockett, R. E. (2006). Bdellovibrio predation in the presence of decoys: Three-way bacterial interactions revealed by mathematical and experimental analyses. Appl Environ Microbiol 72, 6757-6765.
29. Holzapfel, E., Eisner, G., Alami, M., Barrett, C. M., Buchanan, G., Lüke, I., Betton, J. M., Robinson, C., Palmer, T. & other authors (2007). The entire N-terminal half of TatC is involved in twinarginine precursor binding. Biochemistry 46, 2892-2898.
30. Iida, Y., Hobley, L., Lambert, C., Fenton, A. K., Sockett, R. E. & Aizawa, S. (2009). Roles of multiple flagellins in flagellar formation and flagellar growth post bdelloplast lysis in Bdellovibrio bacteriovorus. J Mol Biol 394, 1011-1021.
31. Ize, B., Stanley, N. R., Buchanan, G. & Palmer, T. (2003). Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol Microbiol 48, 1183-1193.
32. Ize, B., Coulthurst, S. J., Hatzixanthis, K., Caldelari, I., Buchanan, G., Barclay, E. C., Richardson, D. J., Palmer, T. & Sargent, F. (2009). Remnant signal peptides on non-exported enzymes: implications for the evolution of prokaryotic respiratory chains. Microbiology 155, 3992-4004.
33. Jack, R. L., Sargent, F., Berks, B. C., Sawers, G. & Palmer, T. (2001). Constitutive expression of Escherichia coli tat genes indicates an important role for the twin-arginine translocase during aerobic and anaerobic growth. J Bacteriol 183, 1801-1804.
34. Kessel, M. & Shilo, M. (1976). Relationship of Bdellovibrio elongation and fission to host cell size. J Bacteriol 128, 477-480.
35. Kimura, Y., Saiga, H., Hamanaka, H. & Matoba, H. (2006). Myxococcus xanthus twin-arginine translocation system is important for growth and development. Arch Microbiol 184, 387-396.
36. Lambert, C. & Sockett, R. E. (2008). Laboratory maintenance of Bdellovibrio. Curr Protoc Microbiol Chapter 7, 7B, 2.
37. Lambert, C., Smith, M. C. & Sockett, R. E. (2003). A novel assay to monitor predator-prey interactions for Bdellovibrio bacteriovorus 109 J reveals a role for methyl-accepting chemotaxis proteins in predation. Environ Microbiol 5, 127-132.
38. Lambert, C., Evans, K. J., Till, R., Hobley, L., Capeness, M., Rendulic, S., Schuster, S. C., Aizawa, S. & Sockett, R. E. (2006). Characterizing the flagellar filament and the role of motility in bacterial preypenetration by Bdellovibrio bacteriovorus. Mol Microbiol 60, 274-286.
39. Lambert, C., Chang, C. Y., Capeness, M. J. & Sockett, R. E. (2010a). The first bite - profiling the predatosome in the bacterial pathogen Bdellovibrio. PLoS ONE 5, e8599.
40. Lambert, C., Ivanov, P. & Sockett, R. E. (2010b). A transcriptional "Scream" early response of E. coli prey to predatory invasion by Bdellovibrio. Curr Microbiol 60, 419-427.
41. Lee, P. A., Tullman-Ercek, D. & Georgiou, G. (2006). The bacterial twin-arginine translocation pathway. Annu Rev Microbiol 60, 373-395.
42. Menon, N. K., Chatelus, C. Y., Dervartanian, M., Wendt, J. C., Shanmugam, K. T., Peck, H. D., Jr & Przybyla, A. E. (1994). Cloning, sequencing, and mutational analysis of the hyb operon encoding Escherichia coli hydrogenase 2. J Bacteriol 176, 4416-4423.
43. Morehouse, K. A., Hobley, L., Capeness, M. & Sockett, R. E. (2011). Three motAB stator gene products in Bdellovibrio bacteriovorus contribute to motility of a single flagellum during predatory and prey-independent growth. J Bacteriol 193, 932-943.
44. Palmer, T., Sargent, F. & Berks, B. C. (2005). Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol 13, 175-180.
45. Pickering, B. S. & Oresnik, I. J. (2010). The twin arginine transport system appears to be essential for viability in Sinorhizobium meliloti. J Bacteriol 192, 5173-5180.
46. Rendulic, S., Jagtap, P., Rosinus, A., Eppinger, M., Baar, C., Lanz, C., Keller, H., Lambert, C., Evans, K. J. & other authors (2004). A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 303, 689-692.
47. Rogers, M., Ekaterinaki, N., Nimmo, E. & Sherratt, D. (1986). Analysis of Tn7 transposition. Mol Gen Genet 205, 550-556.
48. Roschanski, N., Klages, S., Reinhardt, R., Linscheid, M. & Strauch, E. (2011). Identification of genes essential for prey-independent growth of Bdellovibrio bacteriovorus HD100. J Bacteriol 193, 1745-1756.
49. Rose, R. W., Brüser, T., Kissinger, J. C. & 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.
50. Samaluru, H., SaiSree, L. & Reddy, M. (2007). Role of SufI (FtsP) in cell division of Escherichia coli: evidence for its involvement in stabilizing the assembly of the divisome. J Bacteriol 189, 8044-8052.
51. Sargent, F. (2007a). The twin-arginine transport system: moving folded proteins across membranes. Biochem Soc Trans 35, 835-847.
52. Sargent, F. (2007b). Constructing the wonders of the bacterial world: biosynthesis of complex enzymes. Microbiology 153, 633-651.
53. Sargent, F., Bogsch, E. G., Stanley, N. R., Wexler, M., Robinson, C., Berks, B. C. & Palmer, T. (1998). Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J 17, 3640-3650.
54. Sargent, F., Stanley, N. R., Berks, B. C. & Palmer, T. (1999). Secindependent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J Biol Chem 274, 36073-36082.
55. Sargent, F., Gohlke, U., De Leeuw, E., Stanley, N. R., Palmer, T., Saibil, H. R. & Berks, B. C. (2001). Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur J Biochem 268, 3361-3367.
56. Schäfer, A., Tauch, A., Jäger, W., Kalinowski, J., Thierbach, G. & Pühler, A. (1994). Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69-73.
57. Shilo, M. & Bruff, B. (1965). Lysis of Gram-negative bacteria by hostindependent ectoparasitic Bdellovibrio bacteriovorus isolates. J Gen Microbiol 40, 317-328.
58. Simon, R., Priefer, U. & Pühler, A. (1983). A broad host range mobilization system for in vitro genetic engineering: transposon mutagenesis in Gram negative bacteria. Biotechnology 1, 784-791.
59. Sockett, R. E. (2009). Predatory lifestyle of Bdellovibrio bacteriovorus. Annu Rev Microbiol 63, 523-539.
60. Southern, E. M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98, 503-517.
61. Stanley, N. R., Palmer, T. & Berks, B. C. (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.
62. Stanley, N. R., Findlay, K., Berks, B. C. & Palmer, T. (2001). Escherichia coli strains blocked in Tat-dependent protein export exhibit pleiotropic defects in the cell envelope. J Bacteriol 183, 139-144.
63. Stevenson, L. G., Strisovsky, K., Clemmer, K.M., Bhatt, S., Freeman, M. & Rather, P. N. (2007). Rhomboid protease AarA mediates quorumsensing in Providencia stuartii by activating TatA of the twin-arginine translocase. Proc Natl Acad Sci U S A 104, 1003-1008.
64. Steyert, S. R. & Pineiro, S. A. (2007). Development of a novel genetic system to create markerless deletion mutants of Bdellovibrio bacteriovorus. Appl Environ Microbiol 73, 4717-4724.
65. Stolp, H. & Starr, M. P. (1963). Bdellovibrio bacteriovorus gen. et sp. n., a predatory, ectoparasitic, and bacteriolytic microorganism. Antonie van Leeuwenhoek 29, 217-248.
66. Tarry, M., Arends, S. J., Roversi, P., Piette, E., Sargent, F., Berks, B. C., Weiss, D. S. & Lea, S. M. (2009). The Escherichia coli cell division protein and model Tat substrate SufI (FtsP) localizes to the septal ring and has a multicopper oxidase-like structure. J Mol Biol 386, 504-519.
67. Thomashow, M. F. & Rittenberg, S. C. (1979). Descriptive biology of the Bdellovibrios. In Developmental Biology of Prokaryotes. pp. 115-120. Edited by J. H. Parish. Berkeley, CA: University of California Press.
68. Turner, R. J., Papish, A. L. & Sargent, F. (2004). Sequence analysis of bacterial redox enzyme maturation proteins (REMPs). Can J Microbiol 50, 225-238.
69. van der Ploeg, R., Mäder, U., Homuth, G., Schaffer, M., Denham, E. L., Monteferrante, C. G., Miethke, M., Marahiel, M. A., Harwood, C. R. & other authors (2011). Environmental salinity determines the specificity and need for Tat-dependent secretion of the YwbN protein in Bacillus subtilis. PLoS ONE 6, e18140.
70. Vergnes, A., Pommier, J., Toci, R., Blasco, F., Giordano, G. & Magalon, A. (2006). NarJ chaperone binds on two distinct sites of the aponitrate reductase of Escherichia coli to coordinate molybdenum cofactor insertion and assembly. J Biol Chem 281, 2170-2176.
71. Vieira, J. & Messing, J. (1982). The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19, 259-268.
72. Weiner, J. H., Bilous, P. T., Shaw, G. M., Lubitz, S. P., Frost, L., Thomas, G. H., Cole, J. A. & Turner, R. J. (1998). A novel and ubiquitous system for membrane targeting and secretion of cofactorcontaining proteins. Cell 93, 93-101.
73. Yanisch-Perron, C., Vieira, J. & Messing, J. (1985). Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103-119.
74. Yuan, J., Zweers, J. C., van Dijl, J. M. & Dalbey, R. E. (2010). Protein transport across and into cell membranes in bacteria and archaea. Cell Mol Life Sci 67, 179-199.