Flagella-mediated adhesion and extracellular DNA release contribute to biofilm formation and stress tolerance of Campylobacter jejuni

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Svensson, Sarah L ^a   Pryjma, Mark ^a   Gaynor, Erin C ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; DEOXYRIBONUCLEASE; PROTEIN EDNA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; FLHA PROTEIN, BACTERIA; MEMBRANE PROTEIN; PFLA PROTEIN, CAMPYLOBACTER JEJUNI;

ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOFILM; CAMPYLOBACTER JEJUNI; CELL ADHESION; CELL MOTILITY; CELL STRESS; CONFOCAL MICROSCOPY; CYTOLYSIS; EPISTASIS; MOLECULAR MECHANICS; MUTATIONAL ANALYSIS; NONHUMAN; PLANKTON; BACTERIUM ADHERENCE; FLAGELLUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; MUTATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SECRETION (PROCESS); ULTRASTRUCTURE;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CAMPYLOBACTER JEJUNI; DNA, BACTERIAL; EPISTASIS, GENETIC; FLAGELLA; MEMBRANE PROTEINS; MUTATION; PLANKTON; STRESS, PHYSIOLOGICAL;

EID: 84925458828     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106063     Document Type: Article

References (67)

1. Gilbreath JJ, Cody WL, Merrell DS, Hendrixson DR (2011) Change is good: variations in common biological mechanisms in the epsilonproteobacterial genera Campylobacter and Helicobacter. Microbiol Mol Biol Rev 75: 84-132.
2. Szymanski CM, Gaynor EC (2012) How a sugary bug gets through the day: Recent developments in understanding fundamental processes impacting Campylobacter jejuni pathogenesis. Gut Microbes.
3. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, et al. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665-668. (Pubitemid 30104008)
4. O'Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54: 49-79.
5. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
6. Montanaro L, Poggi A, Visai L, Ravaioli S, Campoccia D, et al. (2011) Extracellular DNA in biofilms. Int J Artif Organs 34: 824-831.
7. Mulcahy H, Charron-Mazenod L, Lewenza S (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog 4: e1000213.
8. Ma L, Conover M, Lu H, Parsek MR, Bayles K, et al. (2009) Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 5: e1000354.
9. Thomas VC, Thurlow LR, Boyle D, Hancock LE (2008) Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol 190: 5690-5698.
10. Nguyen D, Joshi-Datar A, Lepine F, Bauerle E, Olakanmi O, et al. (2011) Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334: 982-986.
11. Sanders SQ, Boothe DH, Frank JF, Arnold JW (2007) Culture and detection of Campylobacter jejuni within mixed microbial populations of biofilms on stainless steel. J Food Prot 70: 1379-1385. (Pubitemid 46919658)
12. Trachoo N, Frank JF, Stern NJ (2002) Survival of Campylobacter jejuni in biofilms isolated from chicken houses. J Food Prot 65: 1110-1116. (Pubitemid 34776095)
13. Trachoo N, Frank JF (2002) Effectiveness of chemical sanitizers against Campylobacter jejuni-containing biofilms. J Food Prot 65: 1117-1121. (Pubitemid 34776096)
14. Rollins DM, Colwell RR (1986) Viable but nonculturable stage of Campylobacter jejuni and its role in survival in the natural aquatic environment. Appl Environ Microbiol 52: 531-538. (Pubitemid 16011325)
15. Buswell CM, Herlihy YM, Lawrence LM, McGuiggan JT, Marsh PD, et al. (1998) Extended survival and persistence of Campylobacter spp. in water and aquatic biofilms and their detection by immunofluorescent-antibody and -rRNA staining. Appl Environ Microbiol 64: 733-741. (Pubitemid 28079848)
16. Zimmer M, Barnhart H, Idris U, Lee MD (2003) Detection of Campylobacter jejuni strains in the water lines of a commercial broiler house and their relationship to the strains that colonized the chickens. Avian Dis 47: 101-107. (Pubitemid 36400459)
17. Reeser RJ, Medler RT, Billington SJ, Jost BH, Joens LA (2007) Characterization of Campylobacter jejuni biofilms under defined growth conditions. Appl Environ Microbiol 73: 1908-1913. (Pubitemid 46449074)
18. Reuter M, Mallett A, Pearson BM, van Vliet AH (2010) Biofilm formation by Campylobacter jejuni is increased under aerobic conditions. Appl Environ Microbiol 76: 2122-2128.
19. Svensson SL, Davis LM, MacKichan JK, Allan BJ, Pajaniappan M, et al. (2009) The CprS sensor kinase of the zoonotic pathogen Campylobacter jejuni influences biofilm formation and is required for optimal chick colonization. Mol Microbiol 71: 253-272.
20. Candon HL, Allan BJ, Fraley CD, Gaynor EC (2007) Polyphosphate kinase 1 is a pathogenesis determinant in Campylobacter jejuni. J Bacteriol 189: 8099-8108. (Pubitemid 350178921)
21. Gangaiah D, Liu Z, Arcos J, Kassem, II, Sanad Y, et al. (2010) Polyphosphate kinase 2: a novel determinant of stress responses and pathogenesis in Campylobacter jejuni. PLoS One 5: e12142.
22. McLennan MK, Ringoir DD, Frirdich E, Svensson SL, Wells DH, et al. (2008) Campylobacter jejuni biofilms up-regulated in the absence of the stringent response utilize a calcofluor white-reactive polysaccharide. J Bacteriol 190: 1097-1107. (Pubitemid 351170953)
23. Naito M, Frirdich E, Fields JA, Pryjma M, Li J, et al. (2010) Effects of sequential Campylobacter jejuni 81-176 lipooligosaccharide core truncations on biofilm formation, stress survival, and pathogenesis. J Bacteriol 192: 2182-2192.
24. Rathbun KM, Thompson SA (2009) Mutation of PEB4 alters the outer membrane protein profile of Campylobacter jejuni. FEMS Microbiol Lett 300: 188-194.
25. Joshua GW, Guthrie-Irons C, Karlyshev AV, Wren BW (2006) Biofilm formation in Campylobacter jejuni. Microbiology 152: 387-396. (Pubitemid 43210670)
26. Kalmokoff M, Lanthier P, Tremblay TL, Foss M, Lau PC, et al. (2006) Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J Bacteriol 188: 4312-4320. (Pubitemid 43865750)
27. Grant AJ, Woodward J, Maskell DJ (2006) Development of an ex vivo organ culture model using human gastro-intestinal tissue and Campylobacter jejuni. FEMS Microbiol Lett 263: 240-243. (Pubitemid 44410868)
28. Guerry P (2007) Campylobacter flagella: not just for motility. Trends Microbiol 15: 456-461.
29. Haddock G, Mullin M, MacCallum A, Sherry A, Tetley L, et al. (2010) Campylobacter jejuni 81-176 forms distinct microcolonies on in vitro-infected human small intestinal tissue prior to biofilm formation. Microbiology 156: 3079-3084.
30. Moe KK, Mimura J, Ohnishi T, Wake T, Yamazaki W, et al. (2010) The mode of biofilm formation on smooth surfaces by Campylobacter jejuni . J Vet Med Sci 72: 411-416.
31. Korlath JA, Osterholm MT, Judy LA, Forfang JC, Robinson RA (1985) A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis 152: 592-596. (Pubitemid 15018692)
32. Hendrixson DR, DiRita VJ (2003) Transcription of σ54- dependent but not σ28-dependent flagellar genes in Campylobacter jejuni is associated with formation of the flagellar secretory apparatus. Mol Microbiol 50: 687-702.
33. Hendrixson DR, Akerley BJ, DiRita VJ (2001) Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility. Mol Microbiol 40: 214-224. (Pubitemid 32322874)
34. Frirdich E, Biboy J, Adams C, Lee J, Ellermeier J, et al. (2012) Peptidoglycan-Modifying Enzyme Pgp1 Is Required for Helical Cell Shape and Pathogenicity Traits in Campylobacter jejuni. PLoS Pathog 8: e1002602.
35. Frirdich E, Vermeulen J, Biboy J, Soares F, Taveirne ME, et al. (2014) Peptidoglycan LD-Carboxypeptidase Pgp2 Influences Campylobacter jejuni Helical Cell Shape and Pathogenic Properties, and Provides the Substrate for the DL-Carboxypeptidase Pgp1. J Biol Chem.
36. Apel D, Ellermeier J, Pryjma M, Dirita VJ, Gaynor EC (2012) Characterization of Campylobacter jejuni RacRS reveals a role in the heat shock response, motility, and maintenance of cell length population homogeneity. J Bacteriol.
37. Fujita Y, Yamaguchi K, Kamegaya T, Sato H, Semura K, et al. (2005) A novel mechanism of autolysis in Helicobacter pylori : possible involvement of peptidergic substances. Helicobacter 10: 567-576. (Pubitemid 41668341)
38. Barrero-Tobon AM, Hendrixson DR (2012) Identification and analysis of flagellar coexpressed determinants (Feds) of Campylobacter jejuni involved in colonization. Mol Microbiol.
39. Konkel ME, Klena JD, Rivera-Amill V, Monteville MR, Biswas D, et al. (2004) Secretion of virulence proteins from Campylobacter jejuni is dependent on a functional flagellar export apparatus. J Bacteriol 186: 3296-3303. (Pubitemid 38661524)
40. Rivera-Amill V, Kim BJ, Seshu J, Konkel ME (2001) Secretion of the virulence-associated Campylobacter invasion antigens from Campylobacter jejuni requires a stimulatory signal. J Infect Dis 183: 1607-1616. (Pubitemid 32466698)
41. Yao R, Burr DH, Doig P, Trust TJ, Niu H, et al. (1994) Isolation of motile and non-motile insertional mutants of Campylobacter jejuni: the role of motility in adherence and invasion of eukaryotic cells. Mol Microbiol 14: 883-893. (Pubitemid 24376126)
42. Barrero-Tobon AM, Hendrixson DR (2012) Identification and analysis of flagellar coexpressed determinants (Feds) of Campylobacter jejuni involved in colonization. Mol Microbiol 84: 352-369.
43. Hwang S, Jeon B, Yun J, Ryu S (2011) Roles of RpoN in the resistance of Campylobacter jejuni under various stress conditions. BMC Microbiol 11: 207.
44. Howard SL, Jagannathan A, Soo EC, Hui JP, Aubry AJ, et al. (2009) Campylobacter jejuni glycosylation island important in cell charge, legionaminic acid biosynthesis, and colonization of chickens. Infect Immun 77: 2544-2556.
45. Wright JA, Grant AJ, Hurd D, Harrison M, Guccione EJ, et al. (2009) Metabolite and transcriptome analysis of Campylobacter jejuni in vitro growth reveals a stationary-phase physiological switch. Microbiology 155: 80-94.
46. Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, et al. (2004) Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51: 659-674. (Pubitemid 38233935)
47. Golden NJ, Acheson DW (2002) Identification of motility and autoagglutination Campylobacter jejuni mutants by random transposon mutagenesis. Infect Immun 70: 1761-1771. (Pubitemid 34242175)
48. Karpel RL, Shirley MS, Holt SR (1981) Interaction of the ruthenium red cation with nucleic acid double helices. Biophys Chem 13: 151-165.
49. Theoret JR, Cooper KK, Zekarias B, Roland KL, Law BF, et al. (2012) The Campylobacter jejuni Dps homologue is important for in vitro biofilm formation and cecal colonization of poultry, and may serve as a protective antigen for vaccination. Clin Vaccine Immunol.
50. Mahdavi J, Pirinccioglu N, Oldfield NJ, Carlsohn E, Stoof J, et al. (2014) A novel O-linked glycan modulates Campylobacter jejuni major outer membrane protein-mediated adhesion to human histo-blood group antigens and chicken colonization. Open Biol 4: 130202.
51. Hamilton HL, Dominguez NM, Schwartz KJ, Hackett KT, Dillard JP (2005) Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol Microbiol 55: 1704-1721. (Pubitemid 40445208)
52. Grande R, Di Giulio M, Bessa LJ, Di Campli E, Baffoni M, et al. (2011) Extracellular DNA in Helicobacter pylori biofilm: a backstairs rumour. J Appl Microbiol 110: 490-498.
53. Fournier B, Hooper DC (2000) A new two-component regulatory system involved in adhesion, autolysis, and extracellular proteolytic activity of Staphylococcus aureus. J Bacteriol 182: 3955-3964. (Pubitemid 30436556)
54. Lappann M, Claus H, van Alen T, Harmsen M, Elias J, et al. (2010) A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis . Mol Microbiol 75: 1355-1371.
55. Monteiro C, Fang X, Ahmad I, Gomelsky M, Romling U (2011) Regulation of biofilm components in Salmonella enterica serovar Typhimurium by lytic transglycosylases involved in cell wall turnover. J Bacteriol 193: 6443-6451.
56. Allen KJ, Griffiths MW (2001) Effect of environmental and chemotactic stimuli on the activity of the Campylobacter jejuni flaA sigma(28) promoter. FEMS Microbiol Lett 205: 43-48. (Pubitemid 33135437)
57. Dorel C, Lejeune P, Rodrigue A (2006) The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities? Res Microbiol 157: 306-314.
58. Hung DT, Zhu J, Sturtevant D, Mekalanos JJ (2006) Bile acids stimulate biofilm formation in Vibrio cholerae. Mol Microbiol 59: 193-201.
59. Oh E, Jeon B (2014) Role of Alkyl Hydroperoxide Reductase (AhpC) in the Biofilm Formation of Campylobacter jejuni. PLoS One 9: e87312.
60. Macfarlane S, Furrie E, Macfarlane GT, Dillon JF (2007) Microbial colonization of the upper gastrointestinal tract in patients with Barrett's esophagus. Clin Infect Dis 45: 29-38. (Pubitemid 46984612)
61. Carron MA, Tran VR, Sugawa C, Coticchia JM (2006) Identification of Helicobacter pylori Biofilms in Human Gastric Mucosa. J Gastrointest Surg 10: 712-717. (Pubitemid 43711142)
62. Coticchia JM, Sugawa C, Tran VR, Gurrola J, Kowalski E, et al. (2006) Presence and density of Helicobacter pylori biofilms in human gastric mucosa in patients with peptic ulcer disease. J Gastrointest Surg 10: 883-889. (Pubitemid 43870158)
63. Gaynor EC, Wells DH, MacKichan JK, Falkow S (2005) The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes. Mol Microbiol 56: 8-27. (Pubitemid 40461484)
64. Bayliss CD, Bidmos FA, Anjum A, Manchev VT, Richards RL, et al. (2012) Phase variable genes of Campylobacter jejuni exhibit high mutation rates and specific mutational patterns but mutability is not the major determinant of population structure during host colonization. Nucleic Acids Res.
65. de Boer P, Wagenaar JA, Achterberg RP, van Putten JP, Schouls LM, et al. (2002) Generation of Campylobacter jejuni genetic diversity in vivo. Mol Microbiol 44: 351-359. (Pubitemid 34429741)
66. Lewis K (2000) Programmed death in bacteria. Microbiol Mol Biol Rev 64: 503-514.
67. Ferenci T, Spira B (2007) Variation in stress responses within a bacterial species and the indirect costs of stress resistance. Ann N Y Acad Sci 1113: 105-113. (Pubitemid 350015002)