Biogenesis of outer membrane vesicles in Serratia marcescens is thermoregulated and can be induced by activation of the Rcs phosphorelay system

Journal of Bacteriology

Volumn 194, Issue 12, 2012, Pages 3241-3249

  McMahon, Kenneth J ^a   Castelli, Maria E ^b   Vescovi, Eleonora García ^b   Feldman, Mario F ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; ENTEROBACTERIAL COMMON ANTIGEN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BIOGENESIS; GALLERIA MELLONELLA; INSECT; NONHUMAN; OUTER MEMBRANE; OUTER MEMBRANE VESICLE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; PROTEOMICS; RCS PHOSPHORELAY SYSTEM; SERRATIA MARCESCENS; TEMPERATURE MEASUREMENT; THERMOREGULATION;

ANIMALS; GENE EXPRESSION REGULATION, BACTERIAL; LARVA; LEPIDOPTERA; SECRETORY VESICLES; SERRATIA MARCESCENS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; SURVIVAL ANALYSIS; TEMPERATURE; VIRULENCE;

ENTEROBACTERIACEAE; GALLERIA MELLONELLA; NEGIBACTERIA; OAT MOSAIC VIRUS; SERRATIA; SERRATIA MARCESCENS;

EID: 84864008968     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00016-12     Document Type: Article

References (62)

1. Begic S, Worobec EA. 2008. The role of the Serratia marcescens SdeAB multidrug efflux pump and TolC homologue in fluoroquinolone resistance studied via gene-knockout mutagenesis. Microbiology 154:454- 461.
2. Berthelot P, et al. 1999. Investigation of a nosocomial outbreak due to Serratia marcescens in a maternity hospital. Infect. Control Hosp. Epidemiol. 20:233-236.
3. Beveridge TJ. 1999. Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181:4725- 4733.
4. Bielig H, Dongre M, Zurek B, Wai SN, Kufer TA. 2011. A role for quorum sensing in regulating innate immune responses mediated by Vibrio cholerae outer membrane vesicles (OMVs). Gut Microbes 2:274- 279.
5. Bishop RE. 2005. The lipid A palmitoyltransferase PagP: molecular mechanisms and role in bacterial pathogenesis. Mol. Microbiol. 57:900 -912.
6. Caron F, et al. 2011. From tailor-made to ready-to-wear meningococcal B vaccines: longitudinal study of a clonal meningococcal B outbreak. Lancet Infect. Dis. 11:455- 463.
7. Castelli ME, et al. 2008. Enterobacterial common antigen integrity is a checkpoint for flagellar biogenesis in Serratia marcescens. J. Bacteriol. 190:213-220.
8. Castelli ME, Vescovi EG. 2011. The Rcs signal transduction pathway is triggered by enterobacterial common antigen structure alterations in Serratia marcescens. J. Bacteriol. 193:63-74.
9. Demuth DR, James D, Kowashi Y, Kato S. 2003. Interaction of Actinobacillus actinomycetemcomitans outer membrane vesicles with HL60 cells does not require leukotoxin. Cell. Microbiol. 5:111-121.
10. Dutta S, et al. 2004. Release of Shiga toxin by membrane vesicles in Shigella dysenteriae serotype 1 strains and in vitro effects of antimicrobials on toxin production and release. Microbiol. Immunol. 48:965-969.
11. Ebel W, Vaughn GJ, Peters HK III, Trempy JE. 1997. Inactivation of mdoH leads to increased expression of colanic acid capsular polysaccharide in Escherichia coli. J. Bacteriol. 179:6858-6861.
12. Ellis TN, Kuehn MJ. 2010. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74:81-94.
13. Erbel PJ, et al. 2004. Cyclic enterobacterial common antigen: potential contaminant of bacterially expressed protein preparations. J. Biomol. NMR 29:199 -204.
14. Fedrigo GV, Campoy EM, Di Venanzio G, Colombo MI, Garcia Vescovi E. 2011. Serratia marcescens is able to survive and proliferate in autophagic-like vacuoles inside non-phagocytic cells. PLoS One 6:e24054. doi:10.1371/journal.pone.0024054.
15. Ferrières L, Clarke DJ. 2003. The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the ex-pression of a regulon in response to growth on a solid surface. Mol. Microbiol. 50:1665-1682.
16. Furuta N, et al. 2009. Porphyromonas gingivalis outer membrane vesicles enter human epithelial cells via an endocytic pathway and are sorted to lysosomal compartments. Infect. Immun. 77:4187- 4196.
17. Gankema H, Wensink J, Guinee PA, Jansen WH, Witholt B. 1980. Some characteristics of the outer membrane material released by growing enterotoxigenic Escherichia coli. Infect. Immun. 29:704 -713.
18. Gilbreath JJ, et al. 2012. Enterobacterial common antigen mutants of Salmonella enterica serovar Typhimurium establish a persistent infection and provide protection against subsequent lethal challenge. Infect. Immun. 80:441- 450.
19. Hagiwara D, et al. 2003. Genome-wide analyses revealing a signaling network of the RcsC-YojN-RcsB phosphorelay system in Escherichia coli. J. Bacteriol. 185:5735-5746.
20. Hancock I, Poxton I. 1988. Appendix 1, p 273. In Hancock I, Poxton I (ed), Bacterial cell surface techniques. John Wiley & Sons, Chichester, United Kingdom.
21. Haurat MF, et al. 2011. Selective sorting of cargo proteins into bacterial membrane vesicles. J. Biol. Chem. 286:1269 -1276.
22. Horstman AL, Kuehn MJ. 2000. Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J. Biol. Chem. 275:12489 -12496.
23. Irazoqui JE, et al. 2010. Distinct pathogenesis and host responses during infection of C. elegans by P. aeruginosa and S. aureus. PLoS Pathog. 6:e1000982. doi:10.1371/journal.ppat.1000982.
24. Kadurugamuwa JL, Beveridge TJ. 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.
25. Kajimura J, Rahman A, Rick PD. 2005. Assembly of cyclic enterobacterial common antigen in Escherichia coli K-12. J. Bacteriol. 187:6917- 6927.
26. Kaparakis M, et al. 2010. Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell. Microbiol. 12:372-385.
27. Kaska M, Lysenko O, Chaloupka J. 1976. Exocellular proteases of Serratia marcescens and their toxicity to larvae of Galleria mellonella. Folia Microbiol. (Praha) 21:465- 473.
28. Kato S, Kowashi Y, Demuth DR. 2002. Outer membrane-like vesicles secreted by Actinobacillus actinomycetemcomitans are enriched in leukotoxin. Microb. Pathog. 32:1-13.
29. Kawai E, Akatsuka H, Idei A, Shibatani T, Omori K. 1998. Serratia marcescens S-layer protein is secreted extracellularly via an ATP-binding cassette exporter, the Lip system. Mol. Microbiol. 27:941-952.
30. Kesty NC, Kuehn MJ. 2004. Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J. Biol. Chem. 279:2069 -2076.
31. Kesty NC, Mason KM, Reedy M, Miller SE, Kuehn MJ. 2004. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 23:4538-4549.
32. Khandelwal P, Banerjee-Bhatnagar N. 2003. Insecticidal activity associated with the outer membrane vesicles of Xenorhabdus nematophilus. Appl. Environ. Microbiol. 69:2032-2037.
33. Kuehn MJ, Kesty NC. 2005. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 19:2645-2655.
34. Kulp A, Kuehn MJ. 2010. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol. 64:163-184.
35. Leverrier P, et al. 2011. Crystal structure of the outer membrane protein RcsF, a new substrate for the periplasmic protein-disulfide isomerase DsbC. J. Biol. Chem. 286:16734 -16742.
36. Li Z, Clarke AJ, Beveridge TJ. 1998. Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria. J. Bacteriol. 180:5478 -5483.
37. Lindum PW, et al. 1998. N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. J. Bacteriol. 180: 6384-6388.
38. Majdalani N, Gottesman S. 2005. The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol. 59:379-405.
39. Majdalani N, Heck M, Stout V, Gottesman S. 2005. Role of RcsF in signaling to the Rcs phosphorelay pathway in Escherichia coli. J. Bacteriol. 187:6770-6778.
40. Maragakis LL, et al. 2008. Outbreak of multidrug-resistant Serratia marcescens infection in a neonatal intensive care unit. Infect. Control Hosp. Epidemiol. 29:418-423.
41. Marolda CL, Lahiry P, Vines E, Saldias S, Valvano MA. 2006. Micromethods for the characterization of lipid A-core and O-antigen lipopolysaccharide. Methods Mol. Biol. 347:237-252.
42. Mashburn LM, Whiteley M. 2005. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422- 425.
43. Mashburn-Warren L, et al. 2008. Interaction of quorum signals with outer membrane lipids: insights into prokaryotic membrane vesicle formation. Mol. Microbiol. 69:491-502.
44. Mashburn-Warren LM, Whiteley M. 2006. Special delivery: vesicle trafficking in prokaryotes. Mol. Microbiol. 61:839-846.
45. McBroom AJ, Kuehn MJ. 2007. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 63:545-558.
46. Murdoch SL, et al. 2011. The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J. Bacteriol. 193: 6057-6069.
47. Oster P, et al. 2007. Immunogenicity and safety of a strain-specific MenB OMV vaccine delivered to under 5-year olds in New Zealand. Vaccine 25:3075-3079.
48. Park KS, et al. 2010. Outer membrane vesicles derived from Escherichia coli induce systemic inflammatory response syndrome. PLoS One 5:e11334. doi:10.1371/journal.pone.0011334.
49. Ramos-Morales F, Prieto AI, Beuzon CR, Holden DW, Casadesus J. 2003. Role for Salmonella enterica enterobacterial common antigen in bile resistance and virulence. J. Bacteriol. 185:5328 -5332.
50. Ruiz N, Montero T, Hernandez-Borrell J, Vinas M. 2003. The role of Serratia marcescens porins in antibiotic resistance. Microb. Drug Resist. 9:257-264.
51. Schooling SR, Beveridge TJ. 2006. Membrane vesicles: an overlooked component of the matrices of biofilms. J. Bacteriol. 188:5945-5957.
52. Seitz V, et al. 2003. Identification of immunorelevant genes from greater wax moth (Galleria mellonella) by a subtractive hybridization approach. Dev. Comp. Immunol. 27:207-215.
53. Sharpe SW, Kuehn MJ, Mason KM. 2011. Elicitation of epithelial cellderived immune effectors by outer membrane vesicles of nontypeable Haemophilus influenzae. Infect. Immun. 79:4361- 4369.
54. Shetty A, Chen S, Tocheva EI, Jensen GJ, Hickey WJ. 2011. Nanopods: a new bacterial structure and mechanism for deployment of outer membrane vesicles. PLoS One 6:e20725. doi:10.1371/journal.pone.0020725.
55. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
56. Shibata S, Visick KL. 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.
57. Sledjeski DD, Gottesman S. 1996. Osmotic shock induction of capsule synthesis in Escherichia coli K-12. J. Bacteriol. 178:1204 -1206.
58. Suh B, Bae IK, Kim J, Jeong SH, Yong D, Lee K. 2010. Outbreak of meropenem-resistant Serratia marcescens comediated by chromosomal AmpC beta-lactamase overproduction and outer membrane protein loss. Antimicrob. Agents Chemother. 54:5057-5061.
59. Tsai CM, Frasch CE. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
60. Vidakovics ML, et al. 2010. B cell activation by outer membrane vesicles- a novel virulence mechanism. PLoS Pathog. 6:e1000724. doi: 10.1371/journal.ppat.1000724.
61. Wei JR, Lai HC. 2006. N-acylhomoserine lactone-dependent cell-to-cell communication and social behavior in the genus Serratia. Int. J. Med. Microbiol. 296:117-124.
62. Wensink J, Witholt B. 1981. Outer-membrane vesicles released by normally growing Escherichia coli contain very little lipoprotein. Eur. J. Biochem. 116:331-335.