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Inverse Correlation between Extracellular DNase Activity and Biofilm Formation among Chicken-Derived Campylobacter Strains

  • Jung, Gi Hoon (Department of Food Science and Biotechnology of Animal Resources, Konkuk University) ;
  • Lim, Eun Seob (Department of Food Biotechnology, Korea University of Science and Technology) ;
  • Woo, Min-Ah (Division of Food Safety, Distribution and Standard, Korea Food Research Institute) ;
  • Lee, Joo Young (Food Analysis Center, Korea Food Research Institute) ;
  • Kim, Joo-Sung (Department of Food Biotechnology, Korea University of Science and Technology) ;
  • Paik, Hyun-Dong (Department of Food Science and Biotechnology of Animal Resources, Konkuk University)
  • 투고 : 2017.03.23
  • 심사 : 2017.09.04
  • 발행 : 2017.11.28

초록

Campylobacter jejuni and Campylobacter coli are important foodborne pathogenic bacteria, particularly in poultry meat. In this study, the presence of extracellular DNase activity was investigated for biofilm-deficient Campylobacter strains versus biofilm-forming Campylobacter strains isolated from chickens, to understand the relationship between extracellular DNase activity and biofilm formation. A biofilm-forming reference strain, C. jejuni NCTC11168, was co-incubated with biofilm non-forming strains isolated from raw chickens or their supernatants. The biofilm non-forming strains or supernatants significantly prohibited the biofilm formation of C. jejuni NCTC11168. In addition, the strains degraded pre-formed biofilms of C. jejuni NCTC11168. Degradation of C. jejuni NCTC11168 biofilm was confirmed after treatment with the supernatant of the biofilm non-forming strain 2-1 by confocal laser scanning microscopy. Quantitative analysis of the biofilm matrix revealed reduction of extracellular DNA (16%) and proteins (8.7%) after treatment. Whereas the biofilm-forming strains C. jejuni Y23-5 and C. coli 34-3 isolated from raw chickens and the C. jejuni NCTC11168 reference strain showed no extracellular DNase activity against their own genomic DNA, most biofilm non-forming strains tested, including C. jejuni 2-1, C. coli 34-1, and C. jejuni 63-1, exhibited obvious extracellular DNase activities against their own or 11168 genomic DNA, except for one biofilm non-former, C. jejuni 22-1. Our results suggest that extracellular DNase activity is a common feature suppressing biofilm formation among biofilm non-forming C. jejuni or C. coli strains of chicken origin.

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참고문헌

  1. Allos BM. 2001. Campylobacter jejuni infections: update on emerging issues and trends. Clin. Infect. Dis. 32: 1201-1206. https://doi.org/10.1086/319760
  2. Tam C C, R odrigues L C, V iviani L , Dodds J P, Evans M R, Hunter PR, et al. 2012. Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut 61: 69-77.
  3. Salloway S, Mermel LA, Seamans M, Aspinall GO, Nam Shin JE, Kurjanczyk L, et al. 1996. Miller-Fisher syndrome associated with Campylobacter jejuni bearing lipopolysaccharide molecules that mimic human ganglioside GD3. Infect. Immun. 64: 2945-2949.
  4. Gunther NW, Chen CY. 2009. The biofilm forming potential of bacterial species in the genus Campylobacter. Food Microbiol. 26: 44-51. https://doi.org/10.1016/j.fm.2008.07.012
  5. Joshua GWP, Guthrie-Irons C, Karlyshev AV, Wren BW. 2006. Biofilm formation in Campylobacter jejuni. Microbiology 152: 387-396. https://doi.org/10.1099/mic.0.28358-0
  6. Kalmokoff M, Lanthier P, Tremblay T, Foss M, Lau PC, Sanders G, 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. https://doi.org/10.1128/JB.01975-05
  7. Kim S, Park C, Lee E , Bang W, Kim Y, Kim J. 2017. Biofilm formation of Campylobacter strains isolated from raw chickens and its reduction with DNase I treatment. Food Control 71: 94-100 https://doi.org/10.1016/j.foodcont.2016.06.038
  8. Teh AHT, Lee SM, Dykes GA. 2014. Does Campylobacter jejuni form biofilms in food-related environments? Appl. Environ. Microbiol. 80: 5154-5160 https://doi.org/10.1128/AEM.01493-14
  9. Reuter M, Mallett A, Pearson BM, van Vliet AHM. 2010. Biofilm formation by Campylobacter jejuni is increased under aerobic conditions. Appl. Environ. Microbiol. 76: 2122-2128. https://doi.org/10.1128/AEM.01878-09
  10. Brown HL, Reuter M, Salt LJ, Cross KL, Betts RP, van Vliet AHM. 2014. Chicken juice enhances surface attachment and biofilm formation of Campylobacter jejuni. Appl. Environ. Microbiol. 80: 7053-7060. https://doi.org/10.1128/AEM.02614-14
  11. Sutherland IW. 2001. The biofilm matrix - an immobilized but dynamic microbial environment. Trends Microbiol. 9: 222-227. https://doi.org/10.1016/S0966-842X(01)02012-1
  12. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295: 1487. https://doi.org/10.1126/science.295.5559.1487
  13. Brown HL, Hanman K, Reuter M, Betts RP, van Vliet AHM. 2015. Campylobacter jejuni biofilms contain extracellular DNA and are sensitive to DNase I treatment. Front. Microbiol. 6: 699.
  14. Brown HL, Reuter M, Hanman K, Betts RP, van Vliet AHM. 2015. Prevention of biofilm formation and removal of existing biofilms by extracellular DNases of Campylobacter jejuni. PLoS One 10: e0121680. https://doi.org/10.1371/journal.pone.0121680
  15. Svensson SL, Pryjma M, Gaynor EC. 2014. Flagella-mediated adhesion and extracellular DNA release contribute to biofilm formation and stress tolerance of Campylobacter jejuni. PLoS One 9: e106063. https://doi.org/10.1371/journal.pone.0106063
  16. Kim J, Park C, Kim Y. 2015. Role of flgA for flagellar biosynthesis and biofilm formation of Campylobacter jejuni NCTC11168. J. Microbiol. Biotechnol. 25: 1871-1879. https://doi.org/10.4014/jmb.1504.04080
  17. Okshevsky M, Meyer RL. 2014. Evaluation of fluorescent stains for visualizing extracellular DNA in biofilms. J. Microbiol. Methods 105: 102-104. https://doi.org/10.1016/j.mimet.2014.07.010
  18. Wu J, Xi C. 2009. Evaluation of different methods for extracting extracellular DNA from the biofilm matrix. Appl. Environ. Microbiol. 75: 5390-5395. https://doi.org/10.1128/AEM.00400-09
  19. Branda SS, Vik A, Friedman L, Kolter R. 2005. Biofilms: the matrix revisited. Trends Microbiol. 13: 20-26. https://doi.org/10.1016/j.tim.2004.11.006
  20. Okshevsky M, Regina VR, Meyer RL. 2015. Extracellular DNA as a target for biofilm control. Curr. Opin. Biotechnol. 33: 73-80. https://doi.org/10.1016/j.copbio.2014.12.002
  21. Jakubovics NS, Shields RC, Rajarajan N, Burgess JG. 2013. Life after death: the critical role of extracellular DNA in microbial biofilms. Lett. Appl. Microbiol. 57: 467-475. https://doi.org/10.1111/lam.12134
  22. Mann EE, Rice KC, Boles BR, Endres JL, Ranjit D, Chandramohan L, et al. 2009. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One 4: e5822. https://doi.org/10.1371/journal.pone.0005822
  23. Flemming H, Ridgway H. 2009. Biofilm control: conventional and alternative approaches, pp. 103-117. In Flemming H, Murthy PS, Venkatesan R, Cooksey K (eds.), Marine and Industrial Biofouling. Springer, Berlin-Heidelberg.
  24. Shikongo-Nambabi MNNN, Shoolongela A, Schneider MB. 2012. Control of bacterial contamination during marine fish processing. J. Biol. Life Sci. 3: 1-17.
  25. Chmielewski RAN, Frank JF. 2003. Biofilm formation and control in food processing facilities. Compr. Rev. Food Sci. Food Saf. 2: 22-32. https://doi.org/10.1111/j.1541-4337.2003.tb00012.x
  26. Sofos JN, Geornaras I. 2010. Overview of current meat hygiene and safety risks and summary of recent studies on biofilms, and control of Escherichia coli O157:H7 in nonintact, and Listeria monocytogenes in ready-to-eat, meat products. Meat Sci. 86: 2-14. https://doi.org/10.1016/j.meatsci.2010.04.015
  27. Harvey J, Keenan KP, Gilmour A. 2007. Assessing biofilm formation by Listeria monocytogenes strains. Food Microbiol. 24: 380-392. https://doi.org/10.1016/j.fm.2006.06.006
  28. Costerton JW, Stewart PS. 2001. Battling biofilms. Sci. Am. 285: 74-81.
  29. Mulcahy H, Charron-Mazenod L, Lewenza S. 2008. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4: e1000213. https://doi.org/10.1371/journal.ppat.1000213
  30. Sena-Velez M, Redondo C, Graham JH, Cubero J. 2016. Presence of extracellular DNA during biofilm formation by Xanthomonas citri subsp. citri strains with different host range. PLoS One 11: e0156695. https://doi.org/10.1371/journal.pone.0156695
  31. Jakubovics NS, Burgess JG. 2015. Extracellular DNA in oral microbial biofilms. Microbes Infect. 17: 531-537. https://doi.org/10.1016/j.micinf.2015.03.015
  32. Hymes SR, Randis TM, Sun TY, Ratner AJ. 2013. DNase inhibits Gardnerella vaginalis biofilms in vitro and in vivo. J. Infect. Dis. 207: 1491-1497. https://doi.org/10.1093/infdis/jit047
  33. Okshevsky M, Regina VR, Meyer RL. 2015. Extracellular DNA as a target for biofilm control. Curr. Opin. Biotechnol. 33: 73-80. https://doi.org/10.1016/j.copbio.2014.12.002
  34. Tetz VV, Tetz GV. 2010. Effect of extracellular DNA destruction by DNase I on characteristics of forming biofilms. DNA Cell Biol. 29: 399-405. https://doi.org/10.1089/dna.2009.1011
  35. Tetz GV, Artemenko NK, Tetz VV. 2009. Effect of DNase and antibiotics on biofilm characteristics. Antimicrob. Agents Chemother. 53: 1204-1209. https://doi.org/10.1128/AAC.00471-08
  36. Cho C, Chande A, Gakhar L, Bakaletz LO, Jurcisek JA, Ketterer M, et al. 2015. Role of the nuclease of nontypeable Haemophilus influenzae in dispersal of organisms from biofilms. Infect. Immun. 83: 950-957. https://doi.org/10.1128/IAI.02601-14
  37. Kiedrowski MR, Kavanaugh JS, Malone CL, Mootz JM, Voyich JM, Smeltzer MS, et al. 2011. Nuclease modulates biofilm formation in community-associated methicillin-resistant Staphylococcus aureus. PLoS One 6: e26714. https://doi.org/10.1371/journal.pone.0026714
  38. Seper A, Fengler VHI, Roier S, Wolinski H, Kohlwein SD, Bishop AL, et al. 2011. Extracellular nucleases and extracellular DNA play important roles in Vibrio cholerae biofilm formation. Mol. Microbiol. 82: 1015-1037. https://doi.org/10.1111/j.1365-2958.2011.07867.x
  39. Tran TM, MacIntyre A, Khokhani D, Hawes M, Allen C. 2016. Extracellular DNases of Ralstonia solanacearum modulate biofilms and facilitate bacterial wilt virulence. Environ. Microbiol. 18: 4103-4117. https://doi.org/10.1111/1462-2920.13446
  40. Longhi C, Scoarughi GL, Poggiali F, Cellini A, Carpentieri A, Seganti L, et al. 2008. Protease treatment affects both invasion ability and biofilm formation in Listeria monocytogenes. Microb. Pathog. 45: 45-52. https://doi.org/10.1016/j.micpath.2008.01.007
  41. Park J, Lee J, Kim C, Lee J, Cho MH, Lee J. 2012. Extracellular protease in Actinomycetes culture supernatants inhibits and detaches Staphylococcus aureus biofilm formation. Biotechnol. Lett. 34: 655-661. https://doi.org/10.1007/s10529-011-0825-z
  42. Doern CD, Roberts AL, Hong W, Nelson J, Lukomski S, Swords WE, et al. 2009. Biofilm formation by group A Streptococcus: a role for the streptococcal regulator of virulence (Srv) and streptococcal cysteine protease (SpeB). Microbiology 155: 46-52. https://doi.org/10.1099/mic.0.021048-0
  43. Marti M, Trotonda MP, Tormo-Mas MA, Vergara-Irigaray M, Cheung AL, Lasa I, et al. 2010. Extracellular proteases inhibit protein-dependent biofilm formation in Staphylococcus aureus. Microbes Infect. 12: 55-64. https://doi.org/10.1016/j.micinf.2009.10.005
  44. Tsang LH, Cassat JE, Shaw LN, Beenken KE, Smeltzer MS. 2008. Factors contributing to the biofilm-deficient phenotype of Staphylococcus aureus sarA mutants. PLoS One 3: e3361. https://doi.org/10.1371/journal.pone.0003361
  45. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, et al. 2010. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465:346-349. https://doi.org/10.1038/nature09074
  46. Sugimoto S, Iwamoto T, Takada K, Okuda K, Tajima A, Iwase T, et al. 2013. Staphylococcus epidermidis Esp degrades specific proteins associated with Staphylococcus aureus biofilm formation and host-pathogen interaction. J. Bacteriol. 195:1645-1655. https://doi.org/10.1128/JB.01672-12
  47. Monnappa AK, Dwidar M, Seo JK, Hur J , Mitchell RJ. 2014. Bdellovibrio bacteriovorus inhibits Staphylococcus aureus biofilm formation and invasion into human epithelial cells. Sci. Rep. 4: 3811.
  48. Boehm M, Lind J, Backert S, Tegtmeyer N. 2015. Campylobacter jejuni serine protease HtrA plays an important role in heat tolerance, oxygen resistance, host cell adhesion, invasion, and transmigration. Eur. J. Microbiol. Immunol. (Bp) 5: 68-80. https://doi.org/10.1556/EuJMI-D-15-00003
  49. Pratt LA, Kolter R. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30: 285-293. https://doi.org/10.1046/j.1365-2958.1998.01061.x

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