Predatory activity of Myxococcus xanthus outer-membrane vesicles and properties of their hydrolase cargo

Microbiology (United Kingdom)

Volumn 158, Issue 11, 2012, Pages 2742-2752

  Evans, Alun G L ^a   Davey, Hazel M ^a   Cookson, Alan ^a   Currinn, Heather ^a   Cooke Fox, Gillian ^a   Stanczyk, Paulina J ^a   Whitworth, David E ^a  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYDROLASE; PHOSPHATASE; PROTEINASE;

ARTICLE; BACTERIAL CELL; COMPETITOR SPECIES; ENZYME ACTIVITY; ENZYME KINETICS; ESCHERICHIA COLI; EUKARYOTIC CELL; GENOTYPE; MEMBRANE VESICLE; MYXOCOCCUS XANTHUS; NONHUMAN; PREDATION; PRIORITY JOURNAL;

ANTIBIOSIS; BACTERIAL PROTEINS; CELL MEMBRANE; ESCHERICHIA COLI; HYDROLASES; MYXOCOCCUS XANTHUS; TRANSPORT VESICLES;

ESCHERICHIA COLI; EUKARYOTA; MYXOCOCCUS XANTHUS; NEGIBACTERIA; OAT MOSAIC VIRUS;

EID: 84868313771     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.060343-0     Document Type: Article

References (53)

1. Assunção, P., Antunes, N. T., Rosales, R. S., Poveda, C., Poveda, J. B. & Davey, H. M. (2006). Flow cytometric determination of the effects of antibacterial agents on Mycoplasma agalactiae, Mycoplasma putrefaciens, Mycoplasma capricolum subsp. capricolum, and Mycoplasma mycoides subsp. mycoides large colony type. Antimicrob Agents Chemother 50, 2845-2849.
2. Berleman, J. E. & Kirby, J. R. (2009). Deciphering the hunting strategy of a bacterial wolfpack. FEMS Microbiol Rev 33, 942-957.
3. Berleman, J. E., Chumley, T., Cheung, P. & Kirby, J. R. (2006). Rippling is a predatory behavior in Myxococcus xanthus. J Bacteriol 188, 5888-5895.
4. Bomberger, J. M., Maceachran, D. P., Coutermarsh, B. A., Ye, S., O'Toole, G. A. & Stanton, B. A. (2009). Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog 5, e1000382.
5. Curtis, P. D., Atwood, J., III, Orlando, R. & Shimkets, L. J. (2007). Proteins associated with the Myxococcus xanthus extracellular matrix. J Bacteriol 189, 7634-7642.
6. Davey, H. M. (2011). Life, death, and in-between: meanings and methods in microbiology. Appl Environ Microbiol 77, 5571-5576.
7. Davey, H. M. & Kell, D. B. (1996). Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analyses. Microbiol Rev 60, 641-696.
8. Egea, L., Aguilera, L., Giménez, R., Sorolla, M. A., Aguilar, J., Badía, J. & Baldoma, L. (2007). Role of secreted glyceraldehyde-3-phosphate dehydrogenase in the infection mechanism of enterohemorrhagic and enteropathogenic Escherichia coli: interaction of the extracellular enzyme with human plasminogen and fibrinogen. Int J Biochem Cell Biol 39, 1190-1203.
9. Fiegna, F. & Velicer, G. J. (2003). Competitive fates of bacterial social parasites: persistence and self-induced extinction of Myxococcus xanthus cheaters. Proc Biol Sci 270, 1527-1534.
10. Glaser, P. E. & Gross, R. W. (1995). Rapid plasmenylethanolamineselective fusion of membrane bilayers catalyzed by an isoform of glyceraldehyde-3-phosphate dehydrogenase: discrimination between glycolytic and fusogenic roles of individual isoforms. Biochemistry 34, 12193-12203.
11. Horstman, A. L. & Kuehn, M. J. (2000). Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J Biol Chem 275, 12489-12496.
12. Kadurugamuwa, J. L. & Beveridge, T. J. (1996). Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics. J Bacteriol 178, 2767-2774.
13. Kahnt, J., Aguiluz, K., Koch, J., Treuner-Lange, A., Konovalova, A., Huntley, S., Hoppert, M., Søgaard-Andersen, L. & Hedderich, R. (2010). Profiling the outer membrane proteome during growth and development of the social bacterium Myxococcus xanthus by selective biotinylation and analyses of outer membrane vesicles. J Proteome Res 9, 5197-5208.
14. Kaiser, D. (1979). Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc Natl Acad Sci U S A 76, 5952-5956.
15. Kaiser, D., Robinson, M. & Kroos, L. (2010). Myxobacteria, polarity, and multicellular morphogenesis. Cold Spring Harb Perspect Biol 2, a000380.
16. Khandelwal, P. & Banerjee-Bhatnagar, N. (2003). Insecticidal activity associated with the outer membrane vesicles of Xenorhabdus nematophilus. Appl Environ Microbiol 69, 2032-2037.
17. Kim, J. Y., Doody, A. M., Chen, D. J., Cremona, G. H., Shuler, M. L., Putnam, D. & DeLisa, M. P. (2008). Engineered bacterial outer membrane vesicles with enhanced functionality. J Mol Biol 380, 51-66.
18. Kulp, A. & Kuehn, M. J. (2010). Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64, 163-184.
19. Kümmerli, R. & Brown, S. P. (2010). Molecular and regulatory properties of a public good shape the evolution of cooperation. Proc Natl Acad Sci U S A 107, 18921-18926.
20. Li, Z., Clarke, A. J. & Beveridge, T. J. (1998). Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria. J Bacteriol 180, 5478-5483.
21. López-Amorós, R., Castel, S., Comas-Riu, J. & Vives-Rego, J. (1997). Assessment of E. coli and Salmonella viability and starvation by confocal laser microscopy and flow cytometry using rhodamine 123, DiBAC4(3), propidium iodide, and CTC. Cytometry 29, 298-305.
22. Malamy, M. & Horecker, B. L. (1966). Alkaline phosphatase (crystalline). Methods Enzymol 9, 639-642.
23. Mashburn-Warren, L. M. & Whiteley, M. (2006). Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 61, 839-846.
24. Meiser, P., Bode, H. B. & Müller, R. (2006). The unique DKxanthene secondary metabolite family from the myxobacterium Myxococcus xanthus is required for developmental sporulation. Proc Natl Acad Sci U S A 103, 19128-19133.
25. Meiser, P., Weissman, K. J., Bode, H. B., Krug, D., Dickschat, J. S., Sandmann, A. & Müller, R. (2008). DKxanthene biosynthesis-understanding the basis for diversity-oriented synthesis in myxobacterial secondary metabolism. Chem Biol 15, 771-781.
26. Moraleda-Muñoz, A., Carrero-Lérida, J., Pérez, J. & Muñoz-Dorado, J. (2003). Role of two novel two-component regulatory systems in development and phosphatase expression in Myxococcus xanthus. J Bacteriol 185, 1376-1383.
27. Morgan, A. D., MacLean, R. C., Hillesland, K. L. & Velicer, G. J. (2010). Comparative analysis of Myxococcus predation on soil bacteria. Appl Environ Microbiol 76, 6920-6927.
28. Nakagawa, T., Hirano, Y., Inomata, A., Yokota, S., Miyachi, K., Kaneda, M., Umeda, M., Furukawa, K., Omata, S. & Horigome, T. (2003). Participation of a fusogenic protein, glyceraldehyde-3-phosphate dehydrogenase, in nuclear membrane assembly. J Biol Chem 278, 20395-20404.
29. Nossal, N. G. & Heppel, L. A. (1966). The release of enzymes by osmotic shock from Escherichia coli in exponential phase. J Biol Chem 241, 3055-3062.
30. Palsdottir, H., Remis, J. P., Schaudinn, C., O'Toole, E., Lux, R., Shi, W., McDonald, K. L., Costerton, J. W. & Auer, M. (2009). Threedimensional macromolecular organization of cryofixed Myxococcus xanthus biofilms as revealed by electron microscopic tomography. J Bacteriol 191, 2077-2082.
31. Pham, V. D., Shebelut, C. W., Diodati, M. E., Bull, C. T. & Singer, M. (2005). Mutations affecting predation ability of the soil bacterium Myxococcus xanthus. Microbiology 151, 1865-1874.
32. Pham, V. D., Shebelut, C. W., Jose, I. R., Hodgson, D. A., Whitworth, D. E. & Singer, M. (2006). The response regulator PhoP4 is required for late developmental events in Myxococcus xanthus. Microbiology 152, 1609-1620.
33. Pierson, T., Matrakas, D., Taylor, Y. U., Manyam, G., Morozov, V. N., Zhou, W. & van Hoek, M. L. (2011). Proteomic characterization and functional analysis of outer membrane vesicles of Francisella novicida suggests possible role in virulence and use as a vaccine. J Proteome Res 10, 954-967.
34. Reichenbach, H. & Dworkin, M. (1981). The Order Myxobacterales. In The Prokaryotes, pp. 328-355. Edited by M. P. Starr, H. Stolp, H. G. Truper, A. Balows & H. G. Schlegel. Berlin: Springer-Verlag.
35. Rosenberg, E., Keller, K. H. & Dworkin, M. (1977). Cell densitydependent growth of Myxococcus xanthus on casein. J Bacteriol 129, 770-777.
36. Sambrook, J., Fritsch, E. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
37. Sanders, H. & Feavers, I. M. (2011). Adjuvant properties of meningococcal outer membrane vesicles and the use of adjuvants in Neisseria meningitidis protein vaccines. Expert Rev Vaccines 10, 323-334.
38. Scheer, M., Grote, A., Chang, A., Schomburg, I., Munaretto, C., Rother, M., Söhngen, C., Stelzer, M., Thiele, J. & Schomburg, D. (2011). BRENDA, the enzyme information system in 2011. Nucleic Acids Res 39 (Database issue), D670-D676.
39. Schneiker, S., Perlova, O., Kaiser, O., Gerth, K., Alici, A., Altmeyer, M. O., Bartels, D., Bekel, T., Beyer, S. & other authors (2007). Complete genome sequence of the myxobacterium Sorangium cellulosum. Nat Biotechnol 25, 1281-1289.
40. Silhavy, T. J., Berman, M. L. & Enquist, L. W. (1984). Experiments with Gene Fusions, pp. 209-212. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
41. Tisdale, E. J. (2001). Glyceraldehyde-3-phosphate dehydrogenase is required for vesicular transport in the early secretory pathway. J Biol Chem 276, 2480-2486.
42. Tisdale, E. J., Kelly, C. & Artalejo, C. R. (2004). Glyceraldehyde-3-phosphate dehydrogenase interacts with Rab2 and plays an essential role in endoplasmic reticulum to Golgi transport exclusive of its glycolytic activity. J Biol Chem 279, 54046-54052.
43. Travisano, M. & Velicer, G. J. (2004). Strategies of microbial cheater control. Trends Microbiol 12, 72-78.
44. Troeberg, L. & Nagase, H. (2004). Zymography of metalloproteinases. Curr Protoc Protein Sci 21, 15.
45. Tunio, S. A., Oldfield, N. J., Ala'Aldeen, D. A., Wooldridge, K. G. & Turner, D. P. (2010). The role of glyceraldehyde 3-phosphate dehydrogenase (GapA-1) in Neisseria meningitidis adherence to human cells. BMC Microbiol 10, 280.
46. Velicer, G. J. (2008). Why cooperate? The ecology and evolution of myxobacteria. In Myxobacteria, Multicellularity and Differentiation, pp. 17-40. Edited by D. E. Whitworth. Washington, DC: American Society for Microbiology.
47. Velicer, G. J. & Vos, M. (2009). Sociobiology of the myxobacteria. Annu Rev Microbiol 63, 599-623.
48. Weinberg, R. A. & Zusman, D. R. (1990). Alkaline, acid, and neutral phosphatase activities are induced during development in Myxococcus xanthus. J Bacteriol 172, 2294-2302.
49. Wenzel, S. C. & Müller, R. (2009). The biosynthetic potential of myxobacteria and their impact in drug discovery. Curr Opin Drug Discov Devel 12, 220-230.
50. Whitworth, D. E. (2008). Myxobacteria: Multicellularity and Differentiation. Washington, DC: American Society for Microbiology.
51. Whitworth, D. E. (2011). Myxobacterial vesicles: death at a distance? Adv Appl Microbiol 75, 1-31.
52. Whitworth, D. E., Holmes, A. B., Irvine, A. G., Hodgson, D. A. & Scanlan, D. J. (2008). Phosphate acquisition components of the Myxococcus xanthus Pho regulon are regulated by both phosphate availability and development. J Bacteriol 190, 1997-2003.
53. Yonezawa, H., Osaki, T., Kurata, S., Fukuda, M., Kawakami, H., Ochiai, K., Hanawa, T. & Kamiya, S. (2009). Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol 9, 197.