Skip to main content
SpringerLink
Log in

Studying factors involved in biogenesis of Lysobacter sp. XL1 outer membrane vesicles

  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

The Gram-negative bacterium Lysobacter sp. XL1 produces outer membrane vesicles that are heterogeneous in size, density, and protein composition. One of the subpopulations is secretory vesicles for lytic protease L5 of Lysobacter sp. XL1 (Kudryakova et al. (2015) FEMS Microbiol. Lett., 362, fnv137). Protein L5 was assumed to influence biogenesis of these secretory vesicles that contain it. Using a Pseudomonas fluorescens Q2-87/B expression system, it was shown that the recombinant L5 protein may act as a factor of vesicle biogenesis. This points to a possible involvement of L5 protein in Lysobacter sp. XL1 vesicle biogenesis. Furthermore, it was established that the main phospholipid of Lysobacter sp. XL1 vesicles is cardiolipin, and vesicles are formed predominantly of outer membrane regions enriched with this phospholipid. This indicates that cardiolipin participates in biogenesis of all vesicle subpopulations in Lysobacter sp. XL1.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Chatterjee, S. N., and Das, J. (1967) Electron microscopic observations on the excretion of cell-wall material by Vibrio cholera, J. Gen. Microbiol., 49, 1–11.

    Article  CAS  PubMed  Google Scholar 

  2. Mayrand, D., and Grenier, D. (1989) Biological activities of outer membrane vesicles, Can. J. Microbiol., 35, 607–613.

    Article  CAS  PubMed  Google Scholar 

  3. Kuehn, M. J., and Kesty, N. C. (2005) Bacterial outer membrane vesicles and the host–pathogen interaction, Genes Dev., 19, 2645–2655.

    Article  CAS  PubMed  Google Scholar 

  4. Amano, A., Takeuchi, H., and Furuta, N. (2010) Outer membrane vesicles function as offensive weapons in host–parasite interactions, Microbes Infect., 12, 791–798.

    Article  CAS  PubMed  Google Scholar 

  5. Tashiro, Y., Uchiyama, H., and Nomura, N. (2012) Multifunctional membrane vesicles in Pseudomonas aeruginosa, Environ. Microbiol., 14, 1349–1362.

    Article  CAS  PubMed  Google Scholar 

  6. Kulkarni, H. M., and Jagannadham, M. V. (2014) Biogenesis and multifaceted roles of outer membrane vesicles from Gram-negative bacteria, Microbiology, 160, 2109–2121.

    Article  CAS  PubMed  Google Scholar 

  7. Avila-Calderon, E. D., Araiza-Villanueva, M. G., CancinoDiaz, J. C., Lopez-Villegas, E. O., Sriranganathan, N., Boyle, S. M., and Contreras-Rodriguez, A. (2015) Roles of bacterial membrane vesicles, Arch. Microbiol., 197, 1–10.

    Article  CAS  PubMed  Google Scholar 

  8. Kadurugamuwa, J. L., and Beveridge, T. J. (1995) Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion, J. Bacteriol., 177, 3998–4008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Horstman, A. L., and Kuehn, M. J. (2000) Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles, J. Biol. Chem., 275, 12489–12496.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Roier, S., Blume, T., Klug, L., Wagner, G. E., Elhenawy, W., Zangger, K., Prassl, R., Reidl, J., Daum, G., Feldman, M. F., and Schild, S. (2015) A basis for vaccine development: comparative characterization of Haemophilus influenzae outer membrane vesicles, Int. J. Med. Microbiol., 305, 298–309.

    Article  CAS  PubMed  Google Scholar 

  11. Olofsson, A., Vallstrom, A., Petzold, K., Tegtmeyer, N., Schleucher, J., Carlsson, S., Haas, R., Backert, S., Wai, S. N., Grobner, G., and Arnqvist, A. (2010) Biochemical and functional characterization of Helicobacter pylori vesicles, Mol. Microbiol., 77, 1539–1555.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Perez-Cruz, C., Delgado, L., Lopez-Iglesias, C., and Mercade, E. (2015) Outer-inner membrane vesicles naturally secreted by gram-negative pathogenic bacteria, PLoS One, 10, e0116896.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Lee, E. Y., Choi, D. S., Kim, K. P., and Gho, Y. S. (2008) Proteomics in gram-negative bacterial outer membrane vesicles, Mass Spectrom. Rev., 27, 535–555.

    Article  CAS  PubMed  Google Scholar 

  14. Li, Z., Clarke, A. J., and Beveridge, T. J. (1996) A major autolysin of Pseudomonas aeruginosa: subcellular distribution, potential role in cell growth and division and secretion in surface membrane vesicles, J. Bacteriol., 178, 2479–2488.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ciofu, O., Beveridge, T. J., Kadurugamuwa, J., WaltherRasmußsen, J., and Hoiby, N. (2000) Chromosomal ß-lactamase is packaged into membrane vesicles and secreted from Pseudomonas aeruginosa, J. Antimicrob. Chemother., 45, 9–13.

    Article  CAS  PubMed  Google Scholar 

  16. Kobayashi, H., Uematsu, K., Hirayama, H., and Horikoshi, K. (2000) Novel toluene elimination system in a toluenetolerant microorganism, J. Bacteriol., 182, 6451–6455.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kunsmann, L., Ruter, C., Bauwens, A., Greune, L., Gluder, M., Kemper, B., Fruth, A., Wai, S. N., He, X., Lloubes, R., Schmidt, M. A., Dobrindt, U., Mellmann, A., Karch, H., and Bielaszewska, M. (2015) Virulence from vesicles: novel mechanisms of host cell injury by Escherichia coli O104:H4 outbreak strain, Sci. Rep., 5, 13252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Olsen, I., and Amano, A. (2015) Outer membrane vesicles–offensive weapons or good Samaritans? J. Oral Microbiol., 7, 27468.

    Article  PubMed  Google Scholar 

  19. Gujrati, V., Kim, S., Kim, S. H., Min, J. J., Choy, H. E., Kim, S. C., and Jon, S. (2014) Bioengineered bacterial outer membrane vesicles as cell-specific drug-delivery vehicles for cancer therapy, ACS Nano, 8, 1525–1537.

    Article  CAS  PubMed  Google Scholar 

  20. Mashburn-Warren, L. M., and Whiteley, M. (2006) Special delivery: vesicle trafficking in prokaryotes, Mol. Microbiol., 61, 839–846.

    Article  CAS  PubMed  Google Scholar 

  21. Kulp, A., and Kuehn, M. J. (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles, Annu. Rev. Microbiol., 64, 163–184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Schwechheimer, C., Kulp, A., and Kuehn, M. J. (2014) Modulation of bacterial outer membrane vesicle production by envelope structure and content, BMC Microbiol., 14, 324.

    Google Scholar 

  23. Schwechheimer, C., and Kuehn, M. J. (2015) Outer membrane vesicles from Gram-negative bacteria: biogenesis and functions, Nat. Rev. Microbiol., 13, 605–619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hoekstra, D., Van der Laan, J. W., De Leij, L., and Witholt, B. (1976) Release of outer membrane fragments from normally growing Escherichia coli, Biochim. Biophys. Acta, 455, 889–899.

    Article  CAS  PubMed  Google Scholar 

  25. Wensink, J., and Witholt, B. (1981) Outer membrane vesicles released by normally growing Escherichia coli contain very little lipoprotein, Eur. J. Biochem., 116, 331–335.

    Article  CAS  PubMed  Google Scholar 

  26. Schertzer, J. W., and Whiteley, M. (2012) A bilayer-couple model of bacterial outer membrane vesicle biogenesis, MBio, 3, e00297–11.

  27. Zhou, L., Srisatjaluk, R., Justus, D. E., and Doyle, R. J. (1998) On the origin of membrane vesicles in gram-negative bacteria, FEMS Microbiol. Lett., 163, 223–228.

    Article  CAS  PubMed  Google Scholar 

  28. Hayashi, J., Hamada, N., and Kuramitsu, H. K. (2002) The autolysin of Porphyromonas gingivalis is involved in outer membrane vesicle release, FEMS Microbiol. Lett., 216, 217–222.

    Article  CAS  PubMed  Google Scholar 

  29. Balsalobre, C., Silvan, J. M., Berglund, S., Mizunoe, Y., Uhlin, B. E., and Wai, S. N. (2006) Release of the type I secreted a-haemolysin via outer membrane vesicles from Escherichia coli, Mol. Microbiol., 59, 99–112.

    Article  CAS  PubMed  Google Scholar 

  30. Rompikuntal, P. K., Thay, B., Khan, M. K., Alanko, J., Penttinen, A. M., Asikainen, S., Wai, S. N., and Oscarsson, J. (2012) Perinuclear localization of internalized outer membrane vesicles carrying active cytolethal distending toxin from Aggregatibacter actinomycetemcomitans, Infect. Immun., 80, 31–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Stepnaia, O. A., Severin, A. I., Kudryavtseva, A. I., Krupyanko, V. I., Kozlovsky, A. G., and Kulaev, I. S. (1992) Enzymes of bacteriolytic preparation lysoamidase. Some properties of bacteriolytic proteinase L2, Prikl. Biokhim. Mikrobiol., 28, 666–673.

    Google Scholar 

  32. Stepnaya, O. A., Begunova, E. A., Tsfasman, I. M., and Kulaev, I. S. (1996) Bacteriolytic enzyme preparation lysoamidase: isolation and some physicochemical properties of extracellular muramidase from Xanthomonas sp. bacteria, Biochemistry (Moscow), 61, 471–476.

    Google Scholar 

  33. Muranova, T. A., Krasovskaya, L. A., Tsfasman, I. M., Stepnaya, O. A., and Kulaev, I. S. (2004) Structural investigations and identification of the extracellular bacteriolytic endopeptidase L1 from Lysobacter sp., Biochemistry (Moscow), 69, 501–505.

    Article  CAS  Google Scholar 

  34. Stepnaya, O. A., Tsfasman, I. M., Logvina, I. A., Ryazanova, L. P., Muranova, T. A., and Kulaev, I. S. (2005) Isolation and characterization of a new extracellular bacteriolytic endopeptidase of Lysobacter sp. XL1, Biochemistry (Moscow), 70, 1031–1037.

    Article  CAS  Google Scholar 

  35. Vasilyeva, N. V., Tsfasman, I. M., Suzina, N. E., Stepnaya, O. A., and Kulaev, I. S. (2008) Secretion of bacteriolytic endopeptidase L5 of Lysobacter sp. XL1 into the medium by means of outer membrane vesicles, FEBS J., 275, 3827–3835.

    Article  CAS  PubMed  Google Scholar 

  36. Vasilyeva, N. V., Shishkova, N. A., Marinin, L. I., Ledova, L. A., Tsfasman, I. M., Muranova, T. A., Stepnaya, O. A., and Kulaev, I. S. (2014) Lytic peptidase L5 of Lysobacter sp. XL1 with broad antimicrobial spectrum, J. Mol. Microbiol. Biotechnol., 24, 59–66.

    Article  CAS  PubMed  Google Scholar 

  37. Granovsky, I. E., Kalinin, A. E., Lapteva, Y. S., Latypov, O. R., Vasilyeva, N. V., Tsfasman, I. M., Stepnaya, O. A., Kulaev, I. S., Muranova, T. A., and Krasovskaia, L. A. (2011) Lytic Enzyme AlpB of Bacteria Lysobacter sp. XLI, DNA Fragment Encoding the Lytic Enzyme AlpB of Bacteria Lysobacter sp. XLI, and Purification of the Lytic Enzyme AlpB of Bacteria Lysobacter sp. XLI, RFPatent No. 2408725 [in Russian].

    Google Scholar 

  38. Kudryakova, I. V., Suzina, N. E., and Vasilyeva, N. V. (2015) Biogenesis of Lysobacter sp. XL1 vesicles, FEMS Microbiol. Lett., 362, fnv137.

  39. Lapteva, Y. S., Zolova, O. E., Shlyapnikov, M. G., Tsfasman, I. M., Muranova, T. A., Stepnaya, O. A., Kulaev, I. S., and Granovsky, I. E. (2012) Cloning and expression analysis of genes encoding lytic endopeptidases L1 and L5 from Lysobacter sp. strain XL1, Appl. Environ. Microbiol., 78, 7082–7089.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Tsfasman, I. M., Lapteva, Y. S., Krasovskaya, L. A., Kudryakova, I. V., Vasilyeva, N. V., Granovsky, I. E., and Stepnaya, O. A. (2015) Gene expression of lytic endopeptidases AlpA and AlpB from Lysobacter sp. XL1 in Pseudomonads, J. Mol. Microbiol. Biotechnol., 25, 244–252.

    Article  CAS  PubMed  Google Scholar 

  41. Grenier, D., and Mayrand, D. (1987) Functional characterization of extracellular vesicles produced by Bacteroides gingivalis, Infect. Immun., 55, 111–117.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Osborn, M. J., Gander, J. E., Parisi, E., and Carson, J. (1972) Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane, J. Biol. Chem., 247, 3962–3972.

    CAS  PubMed  Google Scholar 

  43. Ames, G. F. (1968) Lipids of Salmonella typhimurium and Escherichia coli: structure and metabolism, J. Bacteriol., 95, 833–843.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent, J. Biol. Chem., 193, 265–275.

    CAS  PubMed  Google Scholar 

  45. Karkhanis, Y. D., Zeltner, J. Y., Jackson, J. J., and Carlo, D. J. (1978) A new and improved microassay to determine 2-keto-3-deoxyoctonate in lipopolysaccharide of Gramnegative bacteria, Anal. Biochem., 85, 595–601.

    Article  CAS  PubMed  Google Scholar 

  46. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680–685.

    Article  CAS  PubMed  Google Scholar 

  47. Choi, D. S., Kim, D. K., Choi, S. J., Lee, J., Choi, J. P., Rho, S., Park, S. H., Kim, Y. K., Hwang, D., and Gho, Y. S. (2011) Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa, Proteomics, 11, 3424–3429.

    Article  CAS  PubMed  Google Scholar 

  48. Bauman, S. J., and Kuehn, M. J. (2006) Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response, Microbes Infect., 8, 2400–2408.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Tashiro, Y., Ichikawa, S., Shimizu, M., Toyofuku, M., Takaya, N., Nakajima-Kambe, T., Uchiyama, H., and Nomura, N. (2010) Variation of physiochemical properties and cell association activity of membrane vesicles with growth phase in Pseudomonas aeruginosa, Appl. Environ. Microbiol., 76, 3732–3739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lappann, M., Otto, A., Becher, D., and Vogel, U. (2013) Comparative proteome analysis of spontaneous outer membrane vesicles and purified outer membranes of Neisseria meningitides, J. Bacteriol., 195, 4425–4435.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Chowdhury, C., and Jagannadham, M. V. (2013) Virulence factors are released in association with outer membrane vesicles of Pseudomonas syringae pv. tomato T1 during normal growth, Biochim. Biophys. Acta, 1834, 231–239.

    Article  CAS  PubMed  Google Scholar 

  52. Kulkarni, H. M., Swamy, Ch. V., and Jagannadham, M. V. (2014) Molecular characterization and functional analysis of outer membrane vesicles from the Antarctic bacterium Pseudomonas syringae suggest a possible response to environmental conditions, J. Proteome Res., 13, 1345–1358.

    Article  CAS  PubMed  Google Scholar 

  53. Tashiro, Y., Inagaki, A., Shimizu, M., Ichikawa, S., Takaya, N., Nakajima-Kambe, T., Uchiyama, H., and Nomura, N. (2011) Characterization of phospholipids in membrane vesicles derived from Pseudomonas aeruginosa, Biosci. Biotechnol. Biochem., 75, 605–607.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. G. K. Skryabin Institute of Biochemistry and Physiology of Microorganisms of the Russian Academy of Sciences (IBPM RAS), 142290, Pushchino, Moscow Region, Russia

    I. V. Kudryakova, N. E. Suzina, N. G. Vinokurova & N. V. Vasilyeva

  2. State Research Center for Applied Microbiology and Biotechnology, 142279, Obolensk, Moscow Region, Russia

    N. A. Shishkova

Authors
  1. I. V. Kudryakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. E. Suzina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. G. Vinokurova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. A. Shishkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. V. Vasilyeva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. V. Kudryakova.

Additional information

Original Russian Text © I. V. Kudryakova, N. E. Suzina, N. G. Vinokurova, N. A. Shishkova, N. V. Vasilyeva, 2017, published in Biokhimiya, 2017, Vol. 82, No. 4, pp. 677-686.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kudryakova, I.V., Suzina, N.E., Vinokurova, N.G. et al. Studying factors involved in biogenesis of Lysobacter sp. XL1 outer membrane vesicles. Biochemistry Moscow 82, 501–509 (2017). https://doi.org/10.1134/S0006297917040125

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297917040125

Keywords

Search

Navigation