Prevention of biofilm formation and removal of existing biofilms by extracellular dnases of campylobacter jejuni

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Brown, Helen L ^a   Reuter, Mark ^a   Hanman, Kate ^a   Betts, Roy P ^b   Van Vliet, Arnoud H M ^a  

^a INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^b CAMPDEN BRI   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; GENOMIC DNA; PROTEIN EDNASES; UNCLASSIFIED DRUG; 4',6 DIAMIDINO 2 PHENYLINDOLE; CRYSTAL VIOLET; DEOXYRIBONUCLEASE; GREEN FLUORESCENT PROTEIN; INDOLE DERIVATIVE; PRIMER DNA;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM ISOLATION; BACTERIUM MUTANT; BIOFILM; CAMPYLOBACTER JEJUNI; CELL VIABILITY; CULTURE MEDIUM; DNA DEGRADATION; EDNASE GENE; GENE INACTIVATION; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; DRUG EFFECTS; ENZYMOLOGY; EXTRACELLULAR SPACE; FOOD CONTROL; GENETICS; GROWTH, DEVELOPMENT AND AGING; SPECIES DIFFERENCE;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI;

BIOFILMS; CAMPYLOBACTER JEJUNI; DEOXYRIBONUCLEASES; DNA PRIMERS; EXTRACELLULAR SPACE; FOOD MICROBIOLOGY; GENTIAN VIOLET; GREEN FLUORESCENT PROTEINS; INDOLES; SPECIES SPECIFICITY;

EID: 84925688210     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121680     Document Type: Article

References (73)

1. Donlan RM. Biofilms: microbial life on surfaces. Emerg Infect Dis 2002; 8: 881-890. PMID: 12194761
2. McCrate OA, Zhou X, Reichhardt C, Cegelski L. Sum of the parts: composition and architecture of the bacterial extracellular matrix. J Mol Biol 2013; 425: 4286-4294. doi: 10.1016/j.jmb.2013.06.022 PMID: 23827139
3. Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol 2010; 8: 623-633. doi: 10.1038/ nrmicro2415 PMID: 20676145
4. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. Extracellular DNA required for bacterial biofilm formation. Science 2002; 295: 1487. PMID: 11859186
5. Mann EE, Rice KC, Boles BR, Endres JL, Ranjit D, Chandramohan L, et al. Modulation of eDNA Release and Degradation Affects Staphylococcus aureus Biofilm Maturation. PLoS One 2009; 4: e5822. doi: 10.1371/journal.pone.0005822 PMID: 19513119
6. Hymes SR, Randis TM, Sun TY, Ratner AJ. DNase inhibits Gardnerella vaginalis biofilms in vitro and in vivo. J Infect Dis 2013; 207: 1491-1497. doi: 10.1093/infdis/jit047 PMID: 23431033
7. Jakubovics NS, Shields RC, Rajarajan N, Burgess JG. Life after death: the critical role of extracellular DNA in microbial biofilms. Lett Appl Microbiol 2013; 57: 467-475. doi: 10.1111/lam.12134 PMID: 23848166
8. Berends ET, Horswill AR, Haste NM, Monestier M, Nizet V, von Kockritz-Blickwede M. Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J Innate Immun 2010; 2: 576-586. doi: 10.1159/000319909 PMID: 20829609
9. Riyapa D, Buddhisa S, Korbsrisate S, Cuccui J, Wren BW, Stevens MP, et al. Neutrophil extracellular traps exhibit antibacterial activity against Burkholderia pseudomallei and are influenced by bacterial and host factors. Infect Immun 2012; 80: 3921-3929. doi: 10.1128/IAI.00806-12 PMID: 22927051
10. Beenken KE, Spencer H, Griffin LM, Smeltzer MS. Impact of Extracellular Nuclease Production on the Biofilm Phenotype of Staphylococcus aureus under In Vitro and In Vivo Conditions. Infect Immun 2012; 80: 1634-1638. doi: 10.1128/IAI.06134-11 PMID: 22354028
11. Seper A, Fengler VH, Roier S, Wolinski H, Kohlwein SD, Bishop AL, et al. Extracellular nucleases and extracellular DNA play important roles in Vibrio cholerae biofilm formation. Mol Microbiol 2011; 82: 1015-1037. doi: 10.1111/j.1365-2958.2011.07867.x PMID: 22032623
12. Finkel SE, Kolter R. DNA as a Nutrient: Novel Role for Bacterial Competence Gene Homologs. J Bacteriol 2001; 183: 6288-6293. PMID: 11591672
13. Mulcahy H, Charron-Mazenod L, Lewenza S. Pseudomonas aeruginosa produces an extracellular deoxyribonuclease that is required for utilization of DNA as a nutrient source. Environ Microbiol 2010; 12: 1621-1629. doi: 10.1111/j.1462-2920.2010.02208.x PMID: 20370819
14. Lambert C, Sockett RE. Nucleases in Bdellovibrio bacteriovorus contribute towards efficient self-biofilm formation and eradication of preformed prey biofilms. FEMS Microbiol Lett 2013; 340: 109-116. doi: 10. 1111/1574-6968.12075 PMID: 23297829
15. Gaasbeek EJ, Wagenaar JA, Guilhabert MR, van Putten JP, Parker CT, van der Wal FJ. Nucleases encoded by the integrated elements CJIE2 and CJIE4 inhibit natural transformation of Campylobacter jejuni. J Bacteriol 2010; 192: 936-941. doi: 10.1128/JB.00867-09 PMID: 20023031
16. Gaasbeek EJ, Wagenaar JA, Guilhabert MR, Wosten MM, van Putten JP, van der Graaf-van Bloois L, et al. A DNase encoded by integrated element CJIE1 inhibits natural transformation of Campylobacter jejuni. J Bacteriol 2009; 191: 2296-2306. doi: 10.1128/JB.01430-08 PMID: 19151136
17. Tam CC, Rodrigues LC, Viviani L, Dodds JP, Evans MR, Hunter PR, et al. Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut 2012; 61: 69-77. doi: 10.1136/gut.2011.238386 PMID: 21708822
18. Zautner AE, Johann C, Strubel A, Busse C, Tareen AM, Masanta WO, et al. Seroprevalence of campylobacteriosis and relevant post-infectious sequelae. Eur J Clin Microbiol Infect Dis 2014; 33: 1019-1027. doi: 10.1007/s10096-013-2040-4 PMID: 24413899
19. Bronowski C, James CE, Winstanley C. Role of environmental survival in transmission of Campylobacter jejuni. FEMS Microbiol Lett 2014; 356: 8-19. doi: 10.1111/1574-6968.12488 PMID: 24888326
20. Joshua GW, Guthrie-Irons C, Karlyshev AV, Wren BW. Biofilm formation in Campylobacter jejuni. Microbiology 2006; 152: 387-396. PMID: 16436427
21. Sulaeman S, Hernould M, Schaumann A, Coquet L, Bolla JM, De E, et al. Enhanced adhesion of Campylobacter jejuni to abiotic surfaces is mediated by membrane proteins in oxygen-enriched conditions. PloS One 2012; 7: e46402. doi: 10.1371/journal.pone.0046402 PMID: 23029510
22. Guyard-Nicodeme M, Tresse O, Houard E, Jugiau F, Courtillon C, El Manaa K, et al. Characterization of Campylobacter spp. transferred from naturally contaminated chicken legs to cooked chicken slices via a cutting board. Int J Food Microbiol 2013; 164: 7-14. doi: 10.1016/j.ijfoodmicro.2013.03.009 PMID: 23587707
23. Gunther NW, Chen CY. The biofilm forming potential of bacterial species in the genus Campylobacter. Food Microbiol 2009; 26: 44-51. doi: 10.1016/j.fm.2008.07.012 PMID: 19028304
24. Balamurugan S, Nattress FM, Baker LP, Dilts BD. Survival of Campylobacter jejuni on beef and pork under vacuum packaged and retail storage conditions: examination of the role of natural meat microflora on C. jejuni survival. Food Microbiol 2011; 28: 1003-1010. doi: 10.1016/j.fm.2011.01.012 PMID: 21569945
25. Teh KH, Flint S, French N. Biofilm formation by Campylobacter jejuni in controlled mixed-microbial populations. Int J Food Microbiol 2010; 143: 118-124. doi: 10.1016/j.ijfoodmicro.2010.07.037 PMID: 20805009
26. Kalmokoff M, Lanthier P, Tremblay TL, Foss M, Lau PC, Sanders G, et al. Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J Bacteriol 2006; 188: 4312-4320. PMID: 16740937
27. Dingle KE, Colles FM, Wareing DRA, Ure R, Fox AJ, Bolton FE, et al. Multilocus Sequence Typing System for Campylobacter jejuni. J Clin Microbiol 2001; 39: 14-23. PMID: 11136741
28. Fouts DE, Mongodin EF, Mandrell RE, Miller WG, Rasko DA, Ravel J, et al. Major Structural Differences and Novel Potential Virulence Mechanisms from the Genomes of Multiple Campylobacter Species. PLoS Biol 2005; 3: e15. PMID: 15660156
29. Parker CT, Quinones B, Miller WG, Horn ST, Mandrell RE. Comparative genomic analysis of Campylobacter jejuni strains reveals diversity due to genomic elements similar to those present in C. jejuni strain RM1221. J Clin Microbiol 2006; 44: 4125-4135. PMID: 16943349
30. Svensson SL, Davis LM, MacKichan JK, Allan BJ, Pajaniappan M, Thompson SA, et al. The CprS sensor kinase of the zoonotic pathogen Campylobacter jejuni influences biofilm formation and is required for optimal chick colonization. Mol Microbiol 2009; 71: 253-272. doi: 10.1111/j.1365-2958.2008.06534. x PMID: 19017270
31. Frirdich E, Vermeulen J, Biboy J, Soares F, Taveirne ME, Johnson JG, et al. 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 2014; 289: 8007-8018. doi: 10. 1074/jbc.M113.491829 PMID: 24394413
32. Oh E, Jeon B. Role of alkyl hydroperoxide reductase (AhpC) in the biofilm formation of Campylobacter jejuni. PLoS One 2014; 9: e87312. doi: 10.1371/journal.pone.0087312 PMID: 24498070
33. Svensson SL, Pryjma M, Gaynor EC. Flagella-Mediated Adhesion and Extracellular DNA Release Contribute to Biofilm Formation and Stress Tolerance of Campylobacter jejuni. PLoS One 2014; 9: e106063. doi: 10.1371/journal.pone.0106063 PMID: 25166748
34. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, Basham D, et al. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 2000; 403: 665-668. PMID: 10688204
35. Reuter M, Mallett A, Pearson BM, van Vliet AH. Biofilm formation by Campylobacter jejuni is increased under aerobic conditions. Appl Environ Microbiol 2010; 76: 2122-2128. doi: 10.1128/AEM.01878-09 PMID: 20139307
36. Manning G, Duim B, Wassenaar T, Wagenaar JA, Ridley A, Newell DG. Evidence for a genetically stable strain of Campylobacter jejuni. Appl Environ Microbiol 2001; 67: 1185-1189. PMID: 11229909
37. Jackson ME, Pratt JM, Stoker NG, Holland IB. An inner membrane protein N-terminal signal sequence is able to promote efficient localisation of an outer membrane protein in Escherichia coli. EMBO J 1985; 4: 2377-2383. PMID: 3908094
38. Reuter M, van Vliet AHM. Signal balancing by the CetABC and CetZ chemoreceptors controls energy taxis in Campylobacter jejuni. PLoS One 2013; 8: e54390. doi: 10.1371/journal.pone.0054390 PMID: 23382896
39. Brown HL, Reuter M, Salt LJ, Cross KL, Betts RP, van Vliet AHM. Chicken juice enhances surface attachment and biofilm formation of Campylobacter jejuni. Appl Environ Microbiol 2014; 80: 7053-7060. doi: 10.1128/AEM.02614-14 PMID: 25192991
40. van Vliet AHM, Wood A. C., Henderson J., Wooldridge K. G., Ketley JM (1998) Genetic Manipulation of enteric Campylobacter species. In: Williams P., Ketley J., Salmond G, editors. Bacterial Pathogenesis. London: Academic Press. pp. 407-420.
41. Miller WG, Bates AH, Horn ST, Brandl MT, Wachtel MR, Mandrell RE. Detection on surfaces and in Caco-2 cells of Campylobacter jejuni cells transformed with new gfp, yfp, and cfp marker plasmids. Appl Environ Microbiol 2000; 66: 5426-5436. PMID: 11097924
42. Donahue JP, Israel DA, Peek RM, Blaser MJ, Miller GG. Overcoming the restriction barrier to plasmid transformation of Helicobacter pylori. Mol Microbiol 2000; 37: 1066-1074. PMID: 10972825
43. Golden NJ, Acheson DW. Identification of motility and autoagglutination Campylobacter jejuni mutants by random transposon mutagenesis. Infect Immun 2002; 70: 1761-1771. PMID: 11895937
44. Jolley KA, Maiden MC. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010; 11: 595. doi: 10.1186/1471-2105-11-595 PMID: 21143983
45. Gillespie JJ, Wattam AR, Cammer SA, Gabbard JL, Shukla MP, Dalay O, et al. PATRIC: the comprehensive bacterial bioinformatics resource with a focus on human pathogenic species. Infect Immun 2011; 79: 4286-4298. doi: 10.1128/IAI.00207-11 PMID: 21896772
46. Kruczkiewicz P, Mutschall S, Barker D, Thomas J, Van Domselaar G, Gannon VPJ, et al. MIST: a tool for rapid in silico generation of molecular data from bacterial genome sequences. Proc Bioinform 2013 2013: 316-323.
47. Sheppard SK, Didelot X, Jolley KA, Darling AE, Pascoe B, Meric G, et al. Progressive genome-wide introgression in agricultural Campylobacter coli. Mol Ecol 2013; 22: 1051-1064. doi: 10.1111/mec.12162 PMID: 23279096
48. Richards VP, Lefebure T, Pavinski Bitar PD, Stanhope MJ. Comparative characterization of the virulence gene clusters (lipooligosaccharide [LOS] and capsular polysaccharide [CPS]) for Campylobacter coli, Campylobacter jejuni subsp. jejuni and related Campylobacter species. Infect Genet Evol 2013; 14: 200-213. doi: 10.1016/j.meegid.2012.12.010 PMID: 23279811
49. Cody AJ, McCarthy ND, Jansen van Rensburg M, Isinkaye T, Bentley SD, Parkhill J, et al. Real-time genomic epidemiological evaluation of human Campylobacter isolates by use of whole-genome multilocus sequence typing. J Clin Microbiol 2013; 51: 2526-2534. doi: 10.1128/JCM.00066-13 PMID: 23698529
50. Colles FM, Maiden MC. Campylobacter sequence typing databases: applications and future prospects. Microbiology 2012; 158: 2695-2709. doi: 10.1099/mic.0.062000-0 PMID: 22986295
51. Bleumink-Pluym NM, van Alphen LB, Bouwman LI, Wosten MM, van Putten JP. Identification of a functional type VI secretion system in Campylobacter jejuni conferring capsule polysaccharide sensitive cytotoxicity. PLoS Pathog 2013; 9: e1003393. doi: 10.1371/journal.ppat.1003393 PMID: 23737749
52. Teh AH, Lee SM, Dykes GA. Do Campylobacter jejuni Form Biofilms in Food-Related Environments? Appl Environ Microbiol 2014; 80: 5154-5160. doi: 10.1128/AEM.01493-14 PMID: 24928882
53. Clark CG, Chong PM, McCorrister SJ, Mabon P, Walker M, Westmacott GR. DNA sequence heterogeneity of Campylobacter jejuni CJIE4 prophages and expression of prophage genes. PLoS One 2014; 9: e95349. doi: 10.1371/journal.pone.0095349 PMID: 24756024
54. Worrall AF, Connolly BA. The chemical synthesis of a gene coding for bovine pancreatic DNase I and its cloning and expression in Escherichia coli. J Biol Chem 1990; 265: 21889-21895. PMID: 2254338
55. Harmsen M, Lappann M, Knochel S, Molin S. Role of extracellular DNA during biofilm formation by Listeria monocytogenes. Appl Environ Microbiol 2010; 76: 2271-2279. doi: 10.1128/AEM.02361-09 PMID: 20139319
56. Zhao J, Wang Q, Li M, Heijstra BD, Wang S, Liang Q, et al. Escherichia coli toxin gene hipA affects biofilm formation and DNA release. Microbiology 2013; 159: 633-640. doi: 10.1099/mic.0.063784-0 PMID: 23329678
57. Dominiak DM, Nielsen JL, Nielsen PH. Extracellular DNA is abundant and important for microcolony strength in mixed microbial biofilms. Environ Microbiol 2011; 13: 710-721. doi: 10.1111/j.1462-2920. 2010.02375.x PMID: 21118344
58. Pammi M, Liang R, Hicks J, Mistretta TA, Versalovic J. Biofilm extracellular DNA enhances mixed species biofilms of Staphylococcus epidermidis and Candida albicans. BMC Microbiol 2013; 13: 257. doi: 10.1186/1471-2180-13-257 PMID: 24228850
59. Zweig M, Schork S, Koerdt A, Siewering K, Sternberg C, Thormann K, et al. Secreted single-stranded DNA is involved in the initial phase of biofilm formation by Neisseria gonorrhoeae. Environ Microbiol 2014; 16: 1040-1052. doi: 10.1111/1462-2920.12291 PMID: 24119133
60. Nguyen MH, Ojima Y, Sakka M, Sakka K, Taya M. Probing of exopolysaccharides with green fluorescence protein-labeled carbohydrate-binding module in Escherichia coli biofilms and flocs induced by bcsB overexpression. J Biosci Bioeng 2014.
61. Godeke J, Heun M, Bubendorfer S, Paul K, Thormann KM. Roles of two Shewanella oneidensis MR-1 extracellular endonucleases. Appl Environ Microbiol 2011; 77: 5342-5351. doi: 10.1128/AEM.00643-11 PMID: 21705528
62. Focareta T, Manning PA. Distinguishing between the extracellular DNases of Vibrio cholerae and development of a transformation system. Mol Microbiol 1991; 5: 2547-2555. PMID: 1791765
63. Kiedrowski MR, Kavanaugh JS, Malone CL, Mootz JM, Voyich JM, Smeltzer MS, et al. Nuclease modulates biofilm formation in community-associated methicillin-resistant Staphylococcus aureus. PLoS One 2011; 6: e26714. doi: 10.1371/journal.pone.0026714 PMID: 22096493
64. Novotny LA, Amer AO, Brockson ME, Goodman SD, Bakaletz LO. Structural stability of Burkholderia cenocepacia biofilms is reliant on eDNA structure and presence of a bacterial nucleic acid binding protein. PLoS One 2013; 8: e67629. doi: 10.1371/journal.pone.0067629 PMID: 23799151
65. Grande R, Di Giulio M, Bessa LJ, Di Campli E, Baffoni M, Guarnieri S, et al. Extracellular DNA in Helicobacter pylori biofilm: a backstairs rumour. J Appl Microbiol 2011; 110: 490-498. doi: 10.1111/j.1365-2672.2010.04911.x PMID: 21143715
66. Wang H, Huang Y, Wu S, Li Y, Ye Y, Zheng Y, et al. Extracellular DNA Inhibits Salmonella enterica Serovar Typhimurium and S. enterica Serovar Typhi Biofilm Development on Abiotic Surfaces. Curr Microbiol 2014; 68: 262-268. doi: 10.1007/s00284-013-0468-5 PMID: 24126602
67. Swartjes JJTM, Das T, Sharifi S, Subbiahdoss G, Sharma PK, Krom BP, et al. A Functional DNase I Coating to Prevent Adhesion of Bacteria and the Formation of Biofilm. Adv Funct Mater 2013; 23: 2843-2849.
68. Konstan MW, Ratjen F. Effect of dornase alfa on inflammation and lung function: potential role in the early treatment of cystic fibrosis. J Cyst Fibros 2012; 11: 78-83. doi: 10.1016/j.jcf.2011.10.003 PMID: 22093951
69. Thornton RB, Wiertsema SP, Kirkham LA, Rigby PJ, Vijayasekaran S, Coates HL, et al. Neutrophil extracellular traps and bacterial biofilms in middle ear effusion of children with recurrent acute otitis media -a potential treatment target. PLoS One 2013; 8: e53837. doi: 10.1371/journal.pone.0053837 PMID: 23393551
70. Conover MS, Mishra M, Deora R. Extracellular DNA is essential for maintaining Bordetella biofilm integrity on abiotic surfaces and in the upper respiratory tract of mice. PLoS One 2011; 6: e16861. doi: 10. 1371/journal.pone.0016861 PMID: 21347299
71. Jones EA, McGillivary G, Bakaletz LO. Extracellular DNA within a nontypeable Haemophilus influen-zae-induced biofilm binds human beta defensin-3 and reduces its antimicrobial activity. J Innate Immun 2013; 5: 24-38. doi: 10.1159/000339961 PMID: 22922323
72. Pemberton JM, Kidd SP, Schmidt R. Secreted enzymes of Aeromonas. FEMS Microbiol Lett 1997; 152: 1-10. PMID: 9228763
73. Derre-Bobillot A, Cortes-Perez NG, Yamamoto Y, Kharrat P, Couve E, Da Cunha V, et al. Nuclease A (Gbs0661), an extracellular nuclease of Streptococcus agalactiae, attacks the neutrophil extracellular traps and is needed for full virulence. Mol Microbiol 2013; 89: 518-531. doi: 10.1111/mmi.12295 PMID: 23772975