Abstract
Campylobacter jejuni is one of the most common causes of bacterial gastrointestinal food-borne infection worldwide. It has been suggested that biofilm formation may play a role in survival of these bacteria in the environment. In this study, the influence of prior modes of growth (planktonic or sessile), temperatures (37 and 42 °C), and nutrient conditions (nutrient broth and Mueller-Hinton broth) on biofilm formation by eight C. jejuni strains with different antibiotic resistance profiles was examined. The ability of these strains to form biofilm on different abiotic surfaces (stainless steel, glass, and polystyrene) as well as factors potentially associated with biofilm formation (bacterial surface hydrophobicity, auto-aggregation, and initial attachment) was also determined. The results showed that cells grown as sessile culture generally have a greater ability to form biofilm (P < 0.05) compared to their planktonic counterparts. Biofilm was also greater (P < 0.05) in lower nutrient media, while growth at different temperatures affects biofilm formation in a strain-dependent manner. The strains were able to attach and form biofilms on different abiotic surfaces, but none of them demonstrated strong, complex, or structured biofilm formation. There were no clear trends between the bacterial surface hydrophobicity, auto-aggregation, attachment, and biofilm formation by the strains. This finding suggests that environmental factors did affect biofilm formation by C. jejuni, and they are more likely to persist in the environment in the form of mixed-species rather than monospecies biofilms.
Similar content being viewed by others
References
Aydin F, Atabay HI, Akan M (2001) The isolation and characterization of Campylobacter jejuni subsp. jejuni from domestic geese (Anser anser). J Appl Microbiol 90(4):637–642. doi:10.1046/j.1365-2672.2001.01293.x
Baylis CL, MacPhee S, Martin KW, Humphrey TJ, Betts RP (2000) Comparison of three enrichment media for the isolation of Campylobacter spp. from foods. J Appl Microbiol 89(5):884–891. doi:10.1046/j.1365-2672.2000.01203.x
Buswell CM, Herlihy YM, Lawrence LM, McGuiggan JTM, Marsh PD, Keevil CW, Leach SA (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(2):733–741
Collado MC, Meriluoto J, Salminen S (2008) Adhesion and aggregation properties of probiotic and pathogen strains. Eur Food Res Technol 226(5):1065–1073
Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284(5418):1318–1322. doi:10.1126/science.284.5418.1318
Duffy L, Dykes GA (2006) Growth temperature of four Campylobacter jejuni strains influences their subsequent survival in food and water. Lett Appl Microbiol 43(6):596–601. doi:10.1111/j.1472-765X.2006.02019.x
Dykes G, Sampathkumar B, Korber D (2003) Planktonic or biofilm growth affects survival, hydrophobicity and protein expression patterns of a pathogenic Campylobacter jejuni strain. Int J Food Microbiol 89(1):1–10
Gallant CV, Daniels C, Leung JM, Ghosh AS, Young KD, Kotra LP, Burrows LL (2005) Common β-lactamases inhibit bacterial biofilm formation. Mol Microbiol 58(4):1012–1024
Ge B, White DG, McDermott PF, Girard W, Zhao S, Hubert S, Meng J (2003) Antimicrobial-resistant Campylobacter species from retail raw meats. Appl Environ Microbiol 69(5):3005–3007
Goulter RM, Gentle IR, Dykes GA (2010) Characterisation of curli production, cell surface hydrophobicity, autoaggregation and attachment behaviour of Escherichia coli O157. Curr Microbiol 61(3):157–162
Gunther NWI, Chen CY (2009) The biofilm forming potential of bacterial species in the genus Campylobacter. Food Microbiol 26(1):44–51. doi:10.1016/j.fm.2008.07.012
Hanning I, Jarquin R, Slavik M (2008) Campylobacter jejuni as a secondary colonizer of poultry biofilms. J Appl Microbiol 105(4):1199–1208. doi:10.1111/j.1365-2672.2008.03853.x
Jacobs-Reitsma W, Lyhs U, Wagenaar J, Nachamkin I, Szymanski C, Blaser M (2008) Campylobacter in the food supply. Campylobacter (Ed. 3):627–644
Joshua GWP, Guthrie-Irons C, Karlyshev AV, Wren BW (2006) Biofilm formation in Campylobacter jejuni. Microbiology 152(2):387–396. doi:10.1099/mic.0.28358-0
Kalmokoff M, Lanthier P, Tremblay T-L, Foss M, Lau PC, Sanders G, Austin J, Kelly J, Szymanski CM (2006) Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J Bacteriol 188(12):4312–4320. doi:10.1128/jb.01975-05
Keener K, Bashor M, Curtis P, Sheldon B, Kathariou S (2004) Comprehensive review of Campylobacter and poultry processing. Compr Rev Food Sci Food Saf 3(2):105–116
Kumar CG, Anand S (1998) Significance of microbial biofilms in food industry: a review. Int J Food Microbiol 42(1):9–27
Luangtongkum T, Jeon B, Han J, Plummer P, Logue CM, Zhang Q (2009) Antibiotic resistance in Campylobacter: emergence, transmission and persistence
Martínez-Rodriguez A, Kelly AF, Park SF, Mackey BM (2004) Emergence of variants with altered survival properties in stationary phase cultures of Campylobacter jejuni. Int J Food Microbiol 90(3):321–329
May T, Ito A, Okabe S (2009) Induction of multidrug resistance mechanism in Escherichia coli biofilms by interplay between tetracycline and ampicillin resistance genes. Antimicrob Agents Chemother 53(11):4628–4639
Moser I, Schröder W (1997) Hydrophobic characterization of thermophilic Campylobacter species and adhesion to INT 407 cell membranes and fibronectin. Microb Pathog 22(3):155–164. doi:10.1006/mpat.1996.0104
Naves P, del Prado G, Huelves L, Gracia M, Ruiz V, Blanco J, Dahbi G, Blanco M, del Carmen Ponte M, Soriano F (2008) Correlation between virulence factors and in vitro biofilm formation by Escherichia coli strains. Microb Pathog 45(2):86–91
Nguyen VT, Turner MS, Dykes GA (2010) Effect of temperature and contact time on Campylobacter jejuni attachment to, and probability of detachment from, stainless steel. J Food Prot 73(5):832–838
Nguyen VT, Turner MS, Dykes GA (2011) Influence of cell surface hydrophobicity on attachment of Campylobacter to abiotic surfaces. Food Microbiol 28(5):942–950
Nucleo E, Fugazza G, Migliavacca R, Spalla M, Comelli M, Pagani L, Debiaggi M (2010) Differences in biofilm formation and aggregative adherence between β-lactam susceptible and β-lactamases producing P. mirabilis clinical isolates. New Microbiol 33(1):37
Reeser RJ, Medler RT, Billington SJ, Jost BH, Joens LA (2007) Characterization of Campylobacter jejuni biofilms under defined growth conditions. Appl Environ Microbiol 73(6):1908–1913. doi:10.1128/aem.00740-06
Reuter M, Mallett A, Pearson BM, van Vliet AHM (2010) Biofilm formation by Campylobacter jejuni is increased under aerobic conditions. Appl Environ Microbiol 76(7):2122–2128. doi:10.1128/aem.01878-09
Rosenberg M (1981) Bacterial adherence to polystyrene: a replica method of screening for bacterial hydrophobicity. Appl Environ Microbiol 42(2):375–377
Salloway S, Mermel LA, Seamans M, Aspinall GO, Nam Shin JE, Kurjanczyk LA, Penner JL (1996) Miller-Fisher syndrome associated with Campylobacter jejuni bearing lipopolysaccharide molecules that mimic human ganglioside GD3. Infect Immun 64(8):2945–2949
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(6):1379–1385
Skirrow MB (1994) Diseases due to Campylobacter, Helicobacter and related bacteria. J Comp Pathol 111(2):113–149
Skyberg J, Siek K, Doetkott C, Nolan L (2007) Biofilm formation by avian Escherichia coli in relation to media, source and phylogeny. J Appl Microbiol 102(2):548–554
Solomon EB, Hoover DG (1999) Campylobacter jejuni: a bacterial paradox. J Food Saf 19(2):121–136. doi:10.1111/j.1745-4565.1999.tb00239.x
Sommer P, Martin-Rouas C, Mettler E (1999) Influence of the adherent population level on biofilm population, structure and resistance to chlorination. Food Microbiol 16(5):503–515
Teh AHT, Lee SM, Dykes GA (2014) Does Campylobacter jejuni form biofilms in food-related environments? Appl Environ Microbiol 80(17):5154–5160
Teh AHT, Lee SM, Dykes GA (2016) Draft genome sequences of three multiantibiotic-resistant Campylobacter jejuni strains (2865, 2868, and 2871) isolated from poultry at retail outlets in Malaysia. Genome Announc. doi:10.1128/genomeA.00331-16
Teh AHT, Wang Y, Dykes GA (2014) The influence of antibiotic resistance gene carriage on biofilm formation by two Escherichia coli strains associated with urinary tract infections. Can J Microbiol 60(2):105–111
Turonova H, Briandet R, Rodrigues R, Hernould M, Hayek N, Stintzi A, Pazlarova J, Tresse O (2015) Biofilm spatial organization by the emerging pathogen Campylobacter jejuni: comparison between NCTC 11168 and 81-176 strains under microaerobic and oxygen-enriched conditions. Frontiers in Microbiol 6
Wieczorek K, Dykes GA, Osek J, Duffy LL (2013) Antimicrobial resistance and genetic characterization of Campylobacter spp. from three countries. Food Control 34(1):84–91
Young VB, Mansfield L (2005) Campylobacter infection-clinical context. Campylobacter: molecular and cellular biology horizon bioscience, Wymondham, Norfolk, UK:1–12
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Teh, A.H.T., Lee, S.M. & Dykes, G.A. The Influence of Prior Modes of Growth, Temperature, Medium, and Substrate Surface on Biofilm Formation by Antibiotic-Resistant Campylobacter jejuni . Curr Microbiol 73, 859–866 (2016). https://doi.org/10.1007/s00284-016-1134-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-016-1134-5