Effects of the Campylobacter jejuni CJIE1 prophage homologs on adherence and invasion in culture, patient symptoms, and source of infection

BMC Microbiology

Matthew W Gilmour²  Dobryan M Tracz³  Jason Moses³  Barbara Marshall3¹  Frank Pollari¹  Christopher CR Grant³  Clifford G Clark² 

[1] Surveillance Division, Centre for Foodborne, Environmental, and Zoonotic Infectious Diseases, Public Health Agency of Canada, 255 Woodlawn Road West, Unit 120, Guelph, Ontario, N1H 8J1, Canada;Department of Medical Microbiology, Room 543 – 745 Bannatyne Avenue, University of Manitoba, Winnipeg, Manitoba, R3E 0J9, Canada;National Microbiology Laboratory, Public Health Agency of Canada, 1015 Arlington Street, Winnipeg, Manitoba, R3E 3R2, Canada

关键词: Source of infection;    Patient symptoms;    Invasion;    Adherence;    Prophage;    C. jejuni;   

Others  :  1144954
DOI  :  10.1186/1471-2180-12-269

 received in 2012-06-20, accepted in 2012-10-12,  发布年份 2012

【 摘 要 】

Background

Prophages of enteric bacteria are frequently of key importance for the biology, virulence, or host adaptation of their host. Some C. jejuni isolates carry homologs of the CJIE1 (CMLP 1) prophage that carry cargo genes potentially involved in virulence. Possible role(s) of CJIE1 homologs in the biology and virulence of C. jejuni were therefore investigated by using in vitro cell culture assays and by assessing the association of C. jejuni isolates with and without these prophages with patients’ symptoms, with source, and with clonal lineages within the C. jejuni population.

Results

Four C. jejuni isolates, three carrying the CJIE1-like prophage and one without, were tested in cell culture assays for adherence and invasion. Both adherence and invasion of C. jejuni to cells in culture were increased by the presence of the CJIE1-family prophage. Differences in motility and growth rate did not appear to be responsible. The CJIE1 prophage was present in 23% of isolates from human and non-human sources combined that were obtained through sentinel-site surveillance, and the distribution of CJIE1 in this population showed modest clonal associations. There was no correlation between the presence of the CJIE1 prophage in C. jejuni and patient symptoms, although there was some statistical support for lower rates of abdominal pain and fever when the prophage was present. Little evidence was found for a role of the prophage in host adaptation or host specificity.

Conclusion

These biological effects suggest that the presence of the prophage may be a marker for differential virulence of some C. jejuni isolates. Ongoing research into the effects of the prophage on protein expression may provide additional insights into the roles the prophage may play in the biology of its host bacterium.

【 授权许可】

   
2012 Clark et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Fouts DE, Mongodin EF, Mandrell RE, Miller WG, Rasko DA, Ravel J, Brinkac LM, DeBoy RT, Parker CT, Daugherty SC, Durkin AS, Madupu R, Sullivan SA, Shetty JU, Ayodeji MA, Shvartsbeyn A, Schatz SC, Badger JH, Fraser CM, Nelson KE: Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol 2005, 3:0072-0085.
• [2]Parker CT, Quiñones 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.
• [3]Barton C, Ng L-K, Tyler SD, Clark CG: Temperate bacteriophages affect pulsed-field gel electrophoresis patterns of Campylobacter jejuni. J Clin Microbiol 2007, 45:386-391.
• [4]Scott AE, Timms AR, Connerton PL, Carrillo CL, Radzum KA, Connerton IF: Genome dynamics of Campylobacter jejuni in response to bacterio-phage predation. PLoS Pathog 2007, 3:e119.
• [5]Clark CG, Ng LK: Sequence variability of Campylobacter temperate bacteriophages. BMC Microbiol 2008, 8:49. BioMed Central Full Text
• [6]Clark CG: Sequencing of CJIE1 prophages from Campylobacter jejuni reveals the presence of inserted and (or) deleted genes. Can J Microbiol 2011, 57:795-809.
• [7]Clark CG, Taboada EN, Grant CCR, Blakeston C, Pollari F, Marshall B, Rahn K, MacKinnon J, Daignault D, Pillai D, Ng L-K: Comparison of molecular typing methods useful for detecting clusters of Campylobacter jejuni and C. coli isolates through routine surveillance. J Clin Microbiol 2012, 50:798-809.
• [8]Kim J-S, Li J, Barnes IHA, Baltzegar DA, Pajaniappan M, Cullen TW, Trent MS, Burns CM, Thompson SA: Role of the Campylobacter jejuni Cj1461 DNA methyltransferase in regulating virulence characteristics. J Bacteriol 2008, 190:6524-6529.
• [9]Kanipes MI, Holder LC, Corcoran AT, Moran AP, Guerry P: A deep rough mutant of Campylobacter jejuni 81–176 is non-invasive for intestinal epithelial cells. Infect Immun 2004, 72:2452-2455.
• [10]Konkel ME, Larson CL, Flanagan RC: Campylobacter jejuni FlpA binds fibronectin and is required for maximal host cell adherence. J Bacteriol 2010, 192:68-76.
• [11]Sałamaszyńska-Guz A, Klymuszko D: Functional analysis of the Campylobacter jejuni cj0183 and cj0588 genes. Curr Microbiol 2008, 56:592-596.
• [12]Fearnley C, Manning G, Bagnall M, Javed MA, Wassenaar TM, Newell DG: Identification of hyperinvasive Campylobacter jejuni strains isolated from poultry and human clinical cases. J Med Microbiol 2008, 57:570-580.
• [13]MacKichan JK, Gaynor EC, Chang C, Cawthraw S, Newell DG, Miller JF, Falkow S: The Campylobacter jejuni dccRS two-component system is required for optimal in vivo colonization but is dispensible for in vitro growth. Mol Microbiol 2004, 54:1269-1286.
• [14]Guerry P: Campylobacter flagella: not just for motility. Trends Microbiol 2007, 15:456-461.
• [15]Zhu J, Hua X, Hou J, Zhao W: The virulence determinants of Campylobacter jejuni and its ability to colonize hosts. Rev Med Microbiol 2008, 19:13-18.
• [16]Christenson JE, Pacheco SA, Konkel ME: Identification of a Campylobacter jejuni-secreted protein required for maximal invasion of host cells. Mol Microbiol 2009, 73:650-662.
• [17]Rathburn KM, Hall JE, Thompson SA: Cj0569 is a periplasmic peptidyl prolyl cis-trans isomerase involved in Campylobacter jejuni motility, invasion, and colonization. BMC Microbiol 2009, 9:160. BioMed Central Full Text
• [18]McCarthy ND, Colles FM, Dingle KE, Bagnall MC, Manning G, Maiden MCJ, Falush D: Host-associated genetic import in Campylobacter jejuni. Emerg Infect Dis 2007, 13:267-272.
• [19]de Haan CPA, Kivistö R, Hakkinen M, Rautelin H, Hänninen ML: Decreasing trend of overlapping multilocus sequence types between human and chicken Campylobacter jejuni isolates over a decade in Finland. Appl Environ Microbiol 2010, 76:5228-5236.
• [20]Kwan PSL, Birtles A, Bolton FJ, French NP, Robinson SE, Newbold LS, Upton M, Fox AJ: Longitudinal study of the molecular epidemiology of Campylobacter jejuni in cattle on dairy farms. Appl Environ Microbiol 2008, 74:3626-3633.
• [21]Pittenger LG, Frye JG, McNerney V, Reeves J, Haro J, Fedorka-Cray PJ, Harrison MA, Englen MD: Analysis of Campylobacter jejuni whole-genome microarrays: significance of prophage and hypervariable regions for discriminating isolates. Foodborne Pathog Dis 2012, 9:473-479.
• [22]Clark CG, Bryden L, Cuff W, Johnson PL, Jamieson F, Ciebin B, Wang G: Use of the Oxford multilocus sequence typing protocol and sequencing of the flagellin short variable region to characterize isolates from a large outbreak of waterborne Campylobacter sp. strains in Walkerton, Ontario, Canada. J Clin Microbiol 2005, 43:2080-2091.
• [23]Clark CG, Price L, Ahmed R, Woodward DL, Melito PL, Rogers FG, Jamieson F, Ciebin B, Li A, Ellis A: Characterization of waterborne outbreak-associated Campylobacter jejuni, Walkerton, Ontario. Emerg Infect Dis 2003, 9:1232-1241.
• [24]Andrysiak AK, Olson AB, Tracz DM, Doré K, Irwin R, Ng L-K, Gilmour MW: and the Canadian Integrated Program for Antimicrobial Resistance Surveillance Collaborative: Genetic characterization of clinical and agri-food isolates of multi-drug resistantSalmonella entericaserovar Heidelberg from Canada. BMC Microbiol 2008, 8:89. BioMed Central Full Text
• [25]Taboada EN, Acedillo RR, Carrillo CD, Findlay WA, Medeiros DT, Mykytczuk OL, Roberts MJ, Valencia CA, Farber JM, Nash JHE: Large-scale comparative genomics meta-analysis of Campylobacter jejuni isolates reveals low level of genome plasticity. J Clin Microbiol 2004, 42:4566-4576.
• [26]Malik-Kale P, Raphael BH, Parker CT, Joens LA, Klena JD, Quiñones B, Keech AM, Konkel ME: Characterization of genetically matched isolates of Campylobacter jejuni reveals that mutations in genes involved in flagellar biosynthesis alter the organism’s virulence potential. Appl Environ Microbiol 2007, 73:3123-3136.