Vibrio fischeri-derived outer membrane vesicles trigger host development

Cellular Microbiology

Volumn 18, Issue 4, 2016, Pages 488-499

  Aschtgen, Marie Stephanie ^a   Wetzel, Keith ^b   Goldman, William ^b   Mcfall Ngai, Margaret ^a   Ruby, Edward ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Euprymna scolopes; Haemocyte; Immune response; OMV; Symbiosis

Indexed keywords

CYTOTOXIN;

ALIIVIBRIO FISCHERI; ARTICLE; BACTERIAL OUTER MEMBRANE; BLOOD CELL; CELL MIGRATION; CONTROLLED STUDY; EPITHELIUM; HOST; IMMUNE RESPONSE; MACROPHAGE; MEMBRANE VESICLE; MORPHOGENESIS; NONHUMAN; OUTER MEMBRANE VESICLE; PRIORITY JOURNAL; SQUID; SYMBIONT; ANIMAL; ANIMAL STRUCTURES; DECAPODIFORMES; EXOSOME; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SYMBIOSIS;

ALIIVIBRIO FISCHERI; ANIMAL STRUCTURES; ANIMALS; DECAPODIFORMES; EXOSOMES; MORPHOGENESIS; SYMBIOSIS;

EID: 84961203604     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12525     Document Type: Article

References (42)

1. Adin, D.M., Engle, J.T., Goldman, W.E., McFall-Ngai, M.J., and Stabb, E.V. (2009) Mutations in ampG and lytic transglycosylase genes affect the net release of peptidoglycan monomers from Vibrio fischeri. J Bacteriol 191: 2012-2022.
2. Bertani, G. (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62: 293-300.
3. Bielig, H., Rompikuntal, P.K., Dongre, M., Zurek, B., Lindmark, B., Ramstedt, M., et al. (2011) NOD-like receptor activation by outer membrane vesicles from Vibrio cholerae non-O1 non-O139 strains is modulated by the quorum-sensing regulator HapR. Infect Immun 79: 1418-1427.
4. Boettcher, K.J., and Ruby, E.G. (1990) Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J Bacteriol 172: 3701-3706.
5. Boudreau, M.A., Fisher, J.F., and Mobashery, S. (2012) Messenger functions of the bacterial cell wall-derived muropeptides. Biochemistry 51: 2974-2990.
6. Brennan, C.A., Mandel, M.J., Gyllborg, M.C., Thomasgard, K.A., and Ruby, E.G. (2013a) Genetic determinants of swimming motility in the squid light-organ symbiont Vibrio fischeri. MicrobiologyOpen 2: 576-594.
7. Brennan, C.A., DeLoney-Marino, C.R., and Mandel, M.J. (2013b) Chemoreceptor VfcA mediates amino acid chemotaxis in Vibrio fischeri. Appl Environ Microbiol 79: 1889-1896.
8. Brennan, C.A., Hunt, J.R., Kremer, N., Krasity, B.C., Apicella, M.A., McFall-Ngai, M.J., and Ruby, E.G. (2014) A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide. eLife 3: e01579. DOI: 10.7554/eLife.01579.
9. Cookson, B.T., Cho, H.L., Herwaldt, L.A., and Goldman, W.E. (1989) Biological activities and chemical composition of purified tracheal cytotoxin of Bordetella pertussis. Infect Immun 57: 2223-2229.
10. Casadevall, A., and Pirofski, L.-A. (2015) What is a host? Incorporating the microbiota into the damage-response framework. Infect Immun 83: 2-7.
11. Doino, J.A., and McFall-Ngai, M.J. (1995) A transient exposure to symbiosis-competent bacteria induces light organ morphogenesis in the host squid. Biol Bull 189: 347-355.
12. Elhenawy, W., Debelyy, M.O., and Feldman, M.F. (2014) Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles. mBio 5: e00909-14. DOI: 10.1128/mBio.00909-14.
13. Ellis, T.N., and Kuehn, M.J. (2010) Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev 74: 81-94.
14. Foster, J.S., Apicella, M.A., and McFall-Ngai, M.J. (2000) Vibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes symbiotic light organ. Dev Biol 226: 242-254.
15. Foster, J.S., and McFall-Ngai, M.J. (1998) Induction of apoptosis by cooperative bacteria in the morphogenesis of host epithelial tissues. Devel Gene Evol 208: 295-303.
16. Graf, J., Dunlap, P.V., and Ruby, E.G. (1994) Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J Bacteriol 176: 6986-6991.
17. Heath-Heckman, E.A.C., and McFall-Ngai, M.J. (2011) The occurrence of chitin in the hemocytes of invertebrates. Zoology (Jena) 114: 191-198.
18. Johnson, J.W., Fisher, J.F., and Mobashery, S. (2013) Bacterial cell-wall recycling. Ann New York Acad Sci 1277: 54-75.
19. Kaparakis, M., Turnbull, L., Carneiro, L., Firth, S., Coleman, H.A., Parkington, H.C., et al. (2010) Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cellul Microbiol 12: 372-385.
20. Koch, E.J., Miyashiro, T., McFall-Ngai, M.J., and Ruby, E.G. (2014) Features governing symbiont persistence in the squid-vibrio association. Mol Ecol 23: 1624-1634.
21. Kohler, P.L., Hamilton, H.L., Cloud-Hansen, K., and Dillard, J.P. (2007) AtlA functions as a peptidoglycan lytic transglycosylase in the Neisseria gonorrhoeae type IV secretion system. J Bacteriol 189: 5421-5428.
22. Koropatnick, T.A., Engle, J.T., Apicella, M.A., Stabb, E.V., Goldman, W.E., and McFall-Ngai, M.J. (2004) Microbial factor-mediated development in a host-bacterial mutualism. Science 306: 1186-1188.
23. Koropatnick, T.A., Kimbell, J.R., and McFall-Ngai, M.J. (2007) Responses of host hemocytes during the initiation of the squid-vibrio symbiosis. Biol Bull 212: 29-39.
24. Kuehn, M.J., and Kesty, N.C. (2005) Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 19: 2645-2655.
25. Kulp, A., and Kuehn, M.J. (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64: 163-184.
26. Lee, K.H., and Ruby, E.G. (1994) Effect of the squid host on the abundance and distribution of symbiotic Vibrio fischeri in nature. Appl Environ Microbiol 60: 1565-1571.
27. Lee, M.-K., Cho, B.-Y., Lee, S.-J., Kang, J.-Y., Jeong, H.D., Huh, S.H., et al. (2001) Histopathological lesions of Manila clam, Tapes philippinarum, from Hadong and Namhae coastal areas of Korea. Aquaculture 201: 199-209.
28. Mandel, M.J., Schaefer, A.L., Brennan, C.A., Heath-Heckman, E.A.C., DeLoney-Marino, C.R., McFall-Ngai, M.J., and Ruby, E.G. (2012) Squid-derived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri. Appl Environ Microbiol 78: 4620-4626.
29. Mashburn-Warren, L.M., and Whiteley, M. (2006) Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 61: 839-846.
30. McFall-Ngai, M.J. (2014) The importance of microbes in animal development: lessons from the squid-vibrio symbiosis. Annu Rev Microbiol 68: 177-194.
31. McFall-Ngai, M.J., and Ruby, E.G. (1991) Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 254: 1491-1494.
32. Montgomery, M.K., and McFall-Ngai, M.J. (1994) Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Euprymna scolopes. Development 120: 1719-1729.
33. Naughton, L.M., and Mandel, M.J. (2012) Colonization of Euprymna scolopes squid by Vibrio fischeri. JoVE 61: e3758. DOI: 10.3791/3758.
34. Nyholm, S.V., Deplancke, B., Gaskins, H.R., Apicella, M.A., and McFall-Ngai, M.J. (2002) Roles of Vibrio fischeri and nonsymbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ. Appl Environ Microbiol 68: 5113-5122.
35. Nyholm, S.V., Stabb, E.V., Ruby, E.G., and McFall-Ngai, M.J. (2000) Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc Natl Acad Sci U S A 97: 10231-10235.
36. Nyholm, S.V., Stewart, J.J., Ruby, E.G., and McFall-Ngai, M.J. (2009) Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ Microbiol 11: 483-493.
37. Okazaki, T., Okudaira, N., Iwabuchi, K., Fugo, H., and Nagai, T. (2006) Apoptosis and adhesion of hemocytes during molting stage of silkworm, Bombyx mori. Zool Sci 23: 299-304.
38. Reichelt, J.L., and Baumann, P. (1974) Effect of sodium chloride on growth of heterotrophic marine bacteria. Arch Microbiol 97: 329-345.
39. Ruby, E.G., and McFall-Ngai, M.J. (1992) A squid that glows in the night: development of an animal-bacterial mutualism. J Bacteriol 174: 4865-4870.
40. Shen, Y., Torchia, M.L.G., Lawson, G.W., Karp, C.L., Ashwell, J.D., and Mazmanian, S.K. (2012) Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12: 509-520.
41. Shibata, S., and Visick, K.L. (2012) Sensor kinase RscS induces the production of antigenically distinct outer membrane vesicles that depend on the symbiosis polysaccharide locus in Vibrio fischeri. J Bacteriol 194: 185-194.
42. Viala, J., Chaput, C., Boneca, I.G., Cardona, A., Girardin, S.E., Moran, A.P., et al. (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori Cag pathogenicity island. Nature Immunol 5: 1166-1174.