Impact of mucin, bile salts and cholesterol on the virulence of Vibrio anguillarum towards gnotobiotic sea bass (Dicentrarchus labrax) larvae

Veterinary Microbiology

Volumn 175, Issue 1, 2015, Pages 44-49

  Li, Xuan ^a   Bossier, Peter ^a   Dierckens, Kristof ^a   Laureau, Stanislas ^b   Defoirdt, Tom ^a  

^a GHENT UNIVERSITY   (Belgium)

^b Ecloserie marine de Gravelines Voie des Enrochements ^*  (France)

Author keywords

Bile salts; Cholesterol; Cue; Host pathogen interaction; Mucin; Virulence

Indexed keywords

CHOLESTEROL; EXOPOLYSACCHARIDE; FLAGELLIN; GLYCOCHOLIC ACID; METALLOPROTEINASE; METHYLTRANSFERASE; MUCIN; PROTEINASE; TAUROCHOLIC ACID; BILE ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BIOFILM; CHER GENE; CONTROLLED STUDY; EMPA GENE; ENZYME ACTIVITY; EUROPEAN SEA BASS; FLAA GENE; FLEQ GENE; GENE EXPRESSION; GNOTOBIOTICS; HOST PATHOGEN INTERACTION; LARVA; LISTONELLA ANGUILLARUM; NONHUMAN; PHENOTYPE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BASS; DRUG EFFECTS; FISH DISEASE; GENETICS; GERMFREE ANIMAL; MICROBIOLOGY; PATHOGENICITY; VETERINARY; VIBRIO; VIBRIOSIS; VIRULENCE;

DICENTRARCHUS LABRAX; LISTONELLA ANGUILLARUM; SERRANIDAE;

ANIMALS; BASS; BILE ACIDS AND SALTS; CHOLESTEROL; FISH DISEASES; GERM-FREE LIFE; LARVA; MUCINS; PHENOTYPE; VIBRIO; VIBRIO INFECTIONS; VIRULENCE;

EID: 84916210424     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2014.10.033     Document Type: Article

References (33)

1. Austin B., Austin A.D. Bacterial Fish Pathogens: Diseases of Farmed and Wild Fish 2012, 369-388. Springer, New York. fifth ed.
2. Begley M., Gahan C.G.M., Hill C. The interaction between bacteria and bile. FEMS Microbiol. Rev. 2005, 29:625-651.
3. Brackman G., Defoirdt T., Miyamoto C., Bossier P., Van Calenbergh S., Nelis H., Coenye T. Cinnamaldehyde and cinnamaldehyde derivatives reduce virulence in Vibrio spp. by decreasing the DNA-binding activity of the quorum sensing response regulator LuxR. BMC Microbiol. 2008, 8:149.
4. Chatterjee A., Dutta P.K., Chowdhury R. Effect of fatty acids and cholesterol present in bile on expression of virulence factors and motility of Vibrio cholerae. Infect. Immun. 2007, 75:1946-1953.
5. Croxatto A., Lauritz J., Chen C., Milton D.L. Vibrio anguillarum colonization of rainbow trout integument requires a DNA locus involved in exopolysaccharide transport and biosynthesis. Environ. Microbiol. 2007, 9:370-382.
6. Denkin S.M., Nelson D.R. Induction of protease activity in Vibrio anguillarum by gastrointestinal mucus. Appl. Environ. Microbiol. 1999, 65:3555-3560.
7. Dierckens K., Rekecki A., Laureau S., Sorgeloos P., Boon N., Van den Broeck W., Bossier P. Development of a bacterial challenge test for gnotobiotic sea bass (Dicentrarchus labrax) larvae. Environ. Microbiol. 2009, 11:526-533.
8. Forstner J., Forstner G. Gastrointestinal mucus. Physiology of the Gastrointestinal Tract 1994, 1255-1283. Raven Press, New York. L.R. Johnson (Ed.).
9. Frans I., Michiels C.W., Bossier P., Willems K.A., Lievens B., Rediers H. Vibrio anguillarum as a fish pathogen: virulence factors, diagnosis and prevention. J. Fish Dis. 2011, 34:643-661.
10. Garcia T., Otto K., Kjelleberg S., Nelson D.R. Growth of Vibrio anguillarum in salmon intestinal mucus. Appl. Environ. Microbiol. 1997, 63:1034-1039.
11. Gotoh K., Kodama T., Hiyoshi H., Izutsu K., Park K.-S., Dryselius R., Akeda Y., Honda T., Iida T. Bile acid-induced virulence gene expression of Vibrio parahaemolyticus reveals a novel therapeutic potential for bile acid sequestrants. PLoS ONE 2010, 5:e13365.
12. Grisez L., Sorgeloos P., Ollevier F. Mode of infection and spread of Vibrio anguillarum in turbot Scophthalmus maximus larvae after oral challenge through live feed. Dis. Aquat. Organ. 1996, 26:181-187.
13. Gunn J.S. Mechanisms of bacterial resistance and response to bile. Microbes Infect. 2000, 2:907-913.
14. Gupta S., Chowdhury R. Bile affects production of virulence factors and motility of Vibrio cholerae. Infect. Immun. 1997, 65:1131-1134.
15. Han Y., Mo Z., Xiao P., Hao B., Li J., Yang G. Characterization of EmpA protease in Vibrio anguillarum M3. J. Ocean Univ. China 2011, 10:379-384.
16. Karatan E., Watnick P. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol. Mol. Biol. Rev. 2009, 73:310-347.
17. Kim B.-S., Kim J.-S. Cholesterol induce oligomerization of Vibrio vulnificus cytolysin specifically. Exp. Mol. Med. 2002, 34:239-242.
18. Larsen M.H., Larsen J.L., Olsen J.E. Chemotaxis of Vibrio anguillarum to fish mucus: role of the origin of the fish mucus, the fish species and the serogroup of the pathogen. FEMS Microbiol. Ecol. 2001, 38:77-80.
19. Li X., Defoirdt T., Yang Q., Laureau S., Bossier P., Dierckens K. Host-induced increase in larval sea bass mortality in a gnotobiotic challenge test with Vibrio anguillarum. Dis. Aquat. Organ. 2014, 108:211-216.
20. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
21. McCarter L.L. Dual flagellar systems enable motility under different circumstances. J. Mol. Microbiol. Biotechnol. 2004, 7:18-29.
22. Milton D.L., Otoole R., Horstedt P., WolfWatz H. Flagellin A is essential for the virulence of Vibrio anguillarum. J. Bacteriol. 1996, 178:1310-1319.
23. Norqvist A., Hagström Å., Wolf-Watz H. Protection of rainbow trout against vibriosis and furunculosis by the use of attenuated strains of Vibrio anguillarum. Appl. Environ. Microbiol. 1989, 55:1400-1405.
24. O'Toole R., Milton D.L., Wolf-Watz H. Chemotactic motility is required for invasion of the host by the fish pathogen Vibrio anguillarum. Mol. Microbiol. 1996, 19:625-637.
25. O'Toole R., Lundberg S., Fredriksson S.-Å., Jansson A., Nilsson B., Wolf-Watz H. The chemotactic response of Vibrio anguillarum to fish intestinal mucus is mediated by a combination of multiple mucus components. J. Bacteriol. 1999, 181:4308-4317.
26. Osawa R., Arakawa E., Okitsu T., Yamai S., Watanabe H. Levels of thermostable direct hemolysin produced by Vibrio parahaemolyticus O3:K6 and other serovars grown anaerobically with the presence of a bile acid. Curr. Microbiol. 2002, 44:302-305.
27. Pace J.L., Chai T.J., Rossi H.A., Jiang X. Effect of bile on Vibrio parahaemolyticus. Appl. Environ. Microbiol. 1997, 63:2372-2377.
28. Ruwandeepika H.A., Defoirdt T., Bhowmick P.P., Karunasagar I., Bossier P. In vitro and in vivo expression of virulence genes in Vibrio isolates belonging to the Harveyi clade in relation to their virulence towards gnotobiotic brine shrimp (Artemia franciscana). Environ. Microbiol. 2011, 13:506-517.
29. Schuhmacher D.A., Klose K.E. Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J. Bacteriol. 1999, 181:1508-1514.
30. Spanggaard B., Huber I., Nielsen J., Nielsen T., Gram L. Proliferation and location of Vibrio anguillarum during infection of rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis. 2000, 23:423-427.
31. Weber B., Chen C., Milton D.L. Colonization of fish skin is vital for Vibrio anguillarum to cause disease. Environ. Microbiol. Rep. 2010, 2:133-139.
32. Wang S.Y., Lauritz J., Jass J., Milton D.L. Role for the major outer-membrane protein from Vibrio anguillarum in bile resistance and biofilm formation. Microbiology 2003, 149:1061-1071.
33. Yang M., Liu Z., Hughes C., Stern A.M., Wang H., Zhong Z., Kan B., Fenical W., Zhu J. Bile salt-induced intermolecular disulfide bond formation activates Vibrio cholerae virulence. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:2348-2353.