Applied Microscopy

Korean Society of Microscopy (한국현미경학회)
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Visualization of Extracellular Vesicles of Prokaryotes and Eukaryotic Microbes

  • Kim, Ki Woo (School of Ecology and Environmental System, Kyungpook National University)
  • Received : 2018.12.19
  • Accepted : 2018.12.27
  • Published : 2018.12.30
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Abstract

The release of nanoscale membrane-bound vesicles is common in all three domains of life. These vesicles are involved in a variety of biological processes such as cell-to-cell communication, horizontal gene transfer, and substrate transport. Prokaryotes including bacteria and archaea release membrane vesicles (MVs) (20 to 400 nm in diameter) into their extracellular milieu. In spite of structural differences in cell envelope, both Gram-positive and negative bacteria produce MVs that contain the cell membrane of each bacterial species. Archaeal MVs characteristically show surface-layer encircling the vesicles. Filamentous fungi and yeasts as eukaryotic microbes produce bilayered exosomes that have varying electron density. Microbes also form intracellular vesicles and minicells that are similar to MVs and exosomes in shape. Electron and fluorescence microscopy could reveal the presence of DNA in MVs and exosomes. Given the biogenesis of extracellular vesicles from the donor cell, in situ high-resolution microscopy can provide insights on the structural mechanisms underlying the formation and release of microbial extracellular vesicles.

Keywords

References

  1. Bielaszewska M, Ruter C, Bauwens A, Greune L, Jarosch K A, Steil D, Zhang W, He X, Lloubes R, Fruth A, Kim K S, Schmidt M A, Dobrindt U, Mellmann A, and Karch H (2017) Host cell interactions of outer membrane vesicle-associated virulence factors of enterohemorrhagic Escherichia coli O157: intercellular delivery, trafficking and mechanisms of cell injury. PLoS Pathog. 13, e1006159. https://doi.org/10.1371/journal.ppat.1006159
  2. Bitto N J, Chapman R, Pidot S, Costin A, Lo C, Choi J, D'Cruze T, Reynolds E C, Dashper S G, Turnbull L, Whitchurch C B, Stinear T P, Stacey K J, and Ferrero R L (2017) Bacterial membrane vesicles transport their DNA cargo into host cells. Sci. Rep. 7, 7072. https://doi.org/10.1038/s41598-017-07288-4
  3. Bohuszewicz O, Liu J, and Low H H (2016) Membrane remodeling in bacteria. J. Struct. Biol. 196, 3-14. https://doi.org/10.1016/j.jsb.2016.05.010
  4. Chernov V M, Mouzykantov A A, Baranova N B, Medvedeva E S, Grygorieva T Y, Trushin M V, Vishnyakov I E, Sabantsev A V, Borchsenius S N, and Chernova O A (2014) Extracellular membrane vesicles secreted by mycoplasma Acholeplasma laidlawii PG8 are enriched in virulence proteins. J. Proteom. 110, 117-128. https://doi.org/10.1016/j.jprot.2014.07.020
  5. De Silva R P, Puccia R, Rodrigues M L, Oliveira D L, Joffe L S, Cesar G V, Nimrichter L, Goldenberg S, and Alves L R (2015) Extracellular vesicle-mediated export of fungal RNA. Sci. Rep. 5, 7763. https://doi.org/10.1038/srep07763
  6. Deatherage B L and Cookson B T (2012) Membrane vesicle release in bacteria. eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Inf. Immun. 80, 1948-1957. https://doi.org/10.1128/IAI.06014-11
  7. Ellen A F, Albers S-V, Huibers W, Pitcher A, Hobel C F V, Schwarz H, Folea M, Schouten S, Boekema E J, Poolman B, and Driessen A J M (2009) Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components. Extremophiles 13, 67-79. https://doi.org/10.1007/s00792-008-0199-x
  8. Giessen T W and Silver P A (2016) Encapsulation as a strategy for the design of biological compartmentalization. J. Mol. Biol. 428, 916-927. https://doi.org/10.1016/j.jmb.2015.09.009
  9. Ionescu M, Zaini P A, Baccari C, Tran S, Da Silva A M, and Lindow S E (2014) Xylella fastidiosa outer membrane vesicles modulate plant colonization by blocking attachment to surfaces. PNAS 111, E3910-3918. https://doi.org/10.1073/pnas.1414944111
  10. Joffe L S, Nimrichter L, Rodrigues M, and Del Poeta M (2016) Potential roles of fungal extracellular vesicles during infection. mSphere 1, e00099-16.
  11. Knox K W, Vesk M, and Work E (1966) Relation between excreted lipopolysaccharide complexes and surface structures of a lysine-limited culture of Escherichia coli. J. Bacteriol. 92, 1206-1217.
  12. Liu Y, Defourny K A Y, Smid E J, and Abee T (2018) Gram-positive bacterial extracelluar vesicles and their impact on health and disease. Front. Microbiol. 9, 1502. https://doi.org/10.3389/fmicb.2018.01502
  13. Marguet E, Gaudin M, Gauliard E, Fourquaux I, Le Blond du Plouy S, Matsui I, and Forterre P (2013) Membrane vesicles, nanopods and/or nanotubes produced by hyperthermophilic archaea of the genus Thermococcus. Biochem. Soc. Trans. 41, 436-442. https://doi.org/10.1042/BST20120293
  14. Martinez-Penafiel E, Fernandez-Ramirez F, Ishida C, Reyes-Cortes R, Sepulveda-Robles O, Guarneros-Pena G, Bermudez-Cruz R M, and Kameyama L (2012) Overexpression of Ipe protein from the coliphage mEp021 induces pleiotropic effects involving haemolysis by HlyE-containing vesicles and cell death. Biochimie 94, 1262-1273. https://doi.org/10.1016/j.biochi.2012.02.004
  15. Oliveira D L, Nakayasu E S, Joffe L S, Guimaraes A J, Sobreira T J P, Nosanchuk J D, Cordero R J B, Frases S, Casadevall A, Almeida I C, Nimrichter L, and Rodrigues M L (2010) Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS ONE 5, e11113. https://doi.org/10.1371/journal.pone.0011113
  16. Perez-Cruz C, Carrion O, Delgado L, Martinez G, Lopez-Iglesias C, and Mercade E (2013) New type of outer membrane vesicle produced by the Gram-negaive bacterium Shewanella vesiculosa M7T: implications for DNA content. Appl. Environ. Microbiol. 79, 1874-1881. https://doi.org/10.1128/AEM.03657-12
  17. Perez-Cruz C, Delgado L, Lopez-Iglesias C, and Mercade E (2015) Outerinner membrane vesicles naturally secreted by Gram-negative pathogenic bacteria. PLoS ONE 10, e0116896. https://doi.org/10.1371/journal.pone.0116896
  18. Raposo G and Stoorvogel W (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200, 373-383. https://doi.org/10.1083/jcb.201211138
  19. Schwechheimer C and Kuehn M J (2015) Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat. Rev. Microbiol. 13, 605-619. https://doi.org/10.1038/nrmicro3525
  20. Seufferheld M J, Kim K M, Whitfield J, Valerio A, and Caetano-Anolles G (2011) Evolution of vacuolar proton pyrophosphatase domains and volutin granules: clues into the early evolutionalry origin of the acidocalcisome. Biol. Direct 6, 50. https://doi.org/10.1186/1745-6150-6-50
  21. Silva B M A, Prados-Rosales R, Espadas-Moreno J, Wolf J M, Luque-Garcia J L, Goncalves T, and Casadevall A (2014) Characterization of Alternaria infectoria extracelluar vesicles. Med. Mycol. 52, 202-210. https://doi.org/10.1093/mmy/myt003
  22. Sjostrom A E, Sandblad L, Uhlin B E, and Wai S N (2015) Membrane vesicle-mediated release of bacterial RNA. Sci. Rep. 5, 15329. https://doi.org/10.1038/srep15329
  23. Soler N, Marguet E, Verbavatz J-M, and Forterre P (2008) Virus-like vesicles and extracellular DNA produced by hyperthermophilic archaea of the order Thermococcales. Res. Microbiol. 159, 390-399. https://doi.org/10.1016/j.resmic.2008.04.015
  24. Thery C, Ostrowski M, and Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581-593. https://doi.org/10.1038/nri2567
  25. Toyofuku M, Tashiro Y, Hasegawa Y, Kurosawa M, and Nomura N (2015) Bacterial membrane vesicles, an overlooked environmental colloid: biology, environmental perspectives and applications. Adv. Colloid Interface Sci. 226, 65-77. https://doi.org/10.1016/j.cis.2015.08.013
  26. Wang X, Thompson C D, Weidenmaier C, and Lee J C (2018) Release of Staphyloccous aureus extracellular vesicles and their application as a vaccine platform. Nat. Commun. 9, 1379. https://doi.org/10.1038/s41467-018-03847-z