1887

Microbiology Society logo

Volume 167, Issue 4

Editor's Choice Bacteriophage infection of leads to the formation of membrane vesicles via both explosive cell lysis and membrane blebbing Open Access

Read the story behind the paper on the Microbe Post here.

Abstract

Membrane vesicles (MVs) are membrane-bound spherical nanostructures that prevail in all three domains of life. In Gram-negative bacteria, MVs are thought to be produced through blebbing of the outer membrane and are often referred to as outer membrane vesicles (OMVs). We have recently described another mechanism of MV formation in that involves explosive cell-lysis events, which shatters cellular membranes into fragments that rapidly anneal into MVs. Interestingly, MVs are often observed within preparations of lytic bacteriophage, however the source of these MVs and their association with bacteriophage infection has not been explored. In this study we aimed to determine if MV formation is associated with lytic bacteriophage infection. Live super-resolution microscopy demonstrated that explosive cell lysis of cells infected with either bacteriophage T4 or T7, resulted in the formation of MVs derived from shattered membrane fragments. Infection by either bacteriophage was also associated with the formation of membrane blebs on intact bacteria. TEM revealed multiple classes of MVs within phage lysates, consistent with multiple mechanisms of MV formation. These findings suggest that bacteriophage infection may be a major contributor to the abundance of bacterial MVs in nature.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): MVs , OMVs and phage
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001021
2021-04-19
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/167/4/mic001021.html?itemId=/content/journal/micro/10.1099/mic.0.001021&mimeType=html&fmt=ahah

References

  1. Deatherage BL, Cookson BT. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun 2012; 80:1948–1957 [View Article][PubMed]
     [Google Scholar]
  2. Ellis TN, Kuehn MJ. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev 2010; 74:81–94 [View Article][PubMed]
     [Google Scholar]
  3. Domingues S, Nielsen KM. Membrane vesicles and horizontal gene transfer in prokaryotes. Curr Opin Microbiol 2017; 38:16–21 [View Article][PubMed]
     [Google Scholar]
  4. Schooling SR, Beveridge TJ. Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 2006; 188:5945–5957 [View Article][PubMed]
     [Google Scholar]
  5. Kulkarni HM, Nagaraj R, Jagannadham MV. Protective role of E. coli outer membrane vesicles against antibiotics. Microbiol Res 2015; 181:1–7 [View Article][PubMed]
     [Google Scholar]
  6. Urashima A, Sanou A, Yen H, Tobe T. Enterohaemorrhagic Escherichia coli produces outer membrane vesicles as an active defence system against antimicrobial peptide LL-37. Cell Microbiol 2017; 19:e12758 [View Article][PubMed]
     [Google Scholar]
  7. Reyes-Robles T, Dillard RS, Cairns LS, Silva-Valenzuela CA, Housman M et al. Vibrio cholerae outer membrane vesicles inhibit bacteriophage infection. J Bacteriol 2018; 200: [View Article][PubMed]
     [Google Scholar]
  8. Biller SJ, Schubotz F, Roggensack SE, Thompson AW, Summons RE et al. Bacterial vesicles in marine ecosystems. Science 2014; 343:183–186 [View Article][PubMed]
     [Google Scholar]
  9. Toyofuku M, Nomura N, Eberl L. Types and origins of bacterial membrane vesicles. Nat Rev Microbiol 2019; 17:13–24 [View Article][PubMed]
     [Google Scholar]
  10. Turnbull L, Toyofuku M, Hynen AL, Kurosawa M, Pessi G et al. Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms. Nat Commun 2016; 7:11220 [View Article][PubMed]
     [Google Scholar]
  11. Young R. Bacteriophage lysis: mechanism and regulation. Microbiol Rev 1992; 56:430–481 [View Article][PubMed]
     [Google Scholar]
  12. Oliveira H, Melo LDR, Santos SB, Nóbrega FL, Ferreira EC et al. Molecular aspects and comparative genomics of bacteriophage endolysins. J Virol 2013; 87:4558–4570 [View Article][PubMed]
     [Google Scholar]
  13. Clokie MR, Millard AD, Letarov AV, Heaphy S. Phages in nature. Bacteriophage 2011; 1:31–45 [View Article][PubMed]
     [Google Scholar]
  14. Bertani G. Lysogenic versus lytic cycle of phage multiplication. Cold Spring Harb Symp Quant Biol 1953; 18:65–70 [View Article][PubMed]
     [Google Scholar]
  15. Lwoff A. Lysogeny. Bacteriol Rev in press 1953; 17:269–337 [View Article][PubMed]
     [Google Scholar]
  16. Young R. Phage lysis: three steps, three choices, one outcome. J Microbiol 2014; 52:243–258 [View Article][PubMed]
     [Google Scholar]
  17. Summer EJ, Berry J, Tran TAT, Niu L, Struck DK et al. Rz/Rz1 lysis gene equivalents in phages of gram-negative hosts. J Mol Biol 2007; 373:1098–1112 [View Article][PubMed]
     [Google Scholar]
  18. Berry J, Rajaure M, Pang T, Young R. The spanin complex is essential for lambda lysis. J Bacteriol 2012; 194:5667–5674 [View Article][PubMed]
     [Google Scholar]
  19. Schiettekatte O, Vincent AT, Malosse C, Lechat P, Chamot-Rooke J et al. Characterization of LE3 and LE4, the only lytic phages known to infect the spirochete Leptospira. Sci Rep 2018; 8:11781 [View Article][PubMed]
     [Google Scholar]
  20. Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 2005; 3:e144 [View Article][PubMed]
     [Google Scholar]
  21. Guang-Han O, Leang-Chung C, Vellasamy KM, Mariappan V, Li-Yen C et al. Experimental phage therapy for Burkholderia pseudomallei infection. PLoS One 2016; 11:e0158213 [View Article][PubMed]
     [Google Scholar]
  22. Bonilla N, Rojas MI, Netto Flores Cruz G, Hung S-H, Rohwer F, Barr JJ et al. Phage on tap-a quick and efficient protocol for the preparation of bacteriophage laboratory stocks. PeerJ 2016; 4:e2261 [View Article][PubMed]
     [Google Scholar]
  23. Beveridge TJ. Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol 1999; 181:4725–4733 [View Article][PubMed]
     [Google Scholar]
  24. Schwechheimer C, Kuehn MJ. Outer-Membrane vesicles from gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol 2015; 13:605–619 [View Article][PubMed]
     [Google Scholar]
  25. Tsugita A, Inouye M. Purification of bacteriophage T4 lysozyme. J Biol Chem 1968; 243:391–397 [View Article][PubMed]
     [Google Scholar]
  26. Inouye M, Arnheim N, Sternglanz R. Bacteriophage T7 lysozyme is an N-acetylmuramyl-L-alanine amidase. J Biol Chem 1973; 248:7247–7252 [View Article][PubMed]
     [Google Scholar]
  27. Hynen AL, Lazenby JJ, Savva GM, McCaughey LC, Turnbull L et al. Multiple holins contribute to extracellular DNA release in Pseudomonas aeruginosa biofilms. Microbiology 2021; 167: [View Article][PubMed]
     [Google Scholar]
  28. Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V et al. The complete genome sequence of Escherichia coli K-12. Science 1997; 277:1453–1462 [View Article][PubMed]
     [Google Scholar]
  29. Kutter E. Phage host range and efficiency of plating. Methods Mol Biol 2009; 501:141–149 [View Article][PubMed]
     [Google Scholar]
  30. Turnbull L, Whitchurch CB. Motility assay: twitching motility. Methods Mol Biol 2014; 1149:73–86 [View Article][PubMed]
     [Google Scholar]
  31. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012; 9:676–682 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001021
Loading
Bacteriophage infection of Escherichia coli leads to the formation of membrane vesicles via both explosive cell lysis and membrane blebbing
Microbiology 167, 001021 (2021); https://doi.org/10.1099/mic.0.001021
/content/journal/micro/10.1099/mic.0.001021
/content/journal/micro/10.1099/mic.0.001021
Loading

Data & Media loading...

Supplements

Supplementary material 1

Supplementary material 2

Supplementary material 3

Supplementary material 4

Supplementary material 5

Supplementary material 6

Supplementary material 7

Supplementary material 8

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error