1887

Abstract

is a member of the oral microbiota that has been associated with the development of inflammatory bowel diseases. However, the role of the bacterium in disease aetiology remains poorly understood. Here, we examine optimal conditions for the growth of , and the pathogenic potential of this bacterium in human gastrointestinal cells from the upper tract. Further, the presence of in the lower tract of Crohn’s disease (CD) patients undergoing therapy is observed, and the associations of with the abundance of other microbial taxa and compounds they produce are evaluated. strains had the ability to tolerate moderate levels of acidity, adhere to and invade esophageal and gastric cells; however, these properties did not correlate with their pathogenic potential in intestinal cells. The presence of the bacterium in the lower gut of CD patients was associated with an increased relative abundance of and incertae sedis. Short chain fatty acids that can be produced by these microbial species did not appear to be responsible for this association. However, we identified genetic similarity between and Firmicutes, specifically within aspartate and glutamate racemases. The potential pathogenesis of in the upper gastrointestinal tract, and the responsiveness of the bacterium to therapy in a subset of CD patients warrant further investigation into whether this bacterium has a causal role in disease or its presence is incidental.

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2016-08-01
2019-12-06
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References

  1. Andreasen J. J., Andersen L. P., Hartzen S. H.. 1988; In vitro susceptibility of diarrhoea producing Gram negative enteric bacteria to sulfasalazine, 5-aminosalicylic acid, sulfapyridine and four quinolones. APMIS96:568–570 [CrossRef][PubMed]
    [Google Scholar]
  2. Bik E. M., Eckburg P. B., Gill S. R., Nelson K. E., Purdom E. A., Francois F., Perez-Perez G., Blaser M. J., Relman D. A.. 2006; Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci U S A103:732–737 [CrossRef][PubMed]
    [Google Scholar]
  3. Blackett K. L., Siddhi S. S., Cleary S., Steed H., Miller M. H., Macfarlane S., Macfarlane G. T., Dillon J. F.. 2013; Oesophageal bacterial biofilm changes in gastro-oesophageal reflux disease, Barrett's and oesophageal carcinoma: association or causality?. Aliment Pharmacol Ther37:1084–1092 [CrossRef][PubMed]
    [Google Scholar]
  4. Burgos-Portugal J. A., Mitchell H. M., Castaño-Rodríguez N., Kaakoush N. O.. 2014; The role of autophagy in the intracellular survival of Campylobacter concisus . FEBS Open Bio4:301–309 [CrossRef][PubMed]
    [Google Scholar]
  5. Castaño-Rodríguez N., Kaakoush N. O., Lee W. S., Mitchell H. M.. 2015; Dual role of Helicobacter and Campylobacter species in IBD: a systematic review and meta-analysis. Gut doi: 10.1136/gutjnl-2015-310545 [CrossRef][PubMed]
    [Google Scholar]
  6. Chaban B., Ngeleka M., Hill J. E.. 2010; Detection and quantification of 14 Campylobacter species in pet dogs reveals an increase in species richness in feces of diarrheic animals. BMC Microbiol10:73 [CrossRef][PubMed]
    [Google Scholar]
  7. Day A. S., Whitten K. E., Lemberg D. A., Clarkson C., Vitug-Sales M., Jackson R., Bohane T. D.. 2006; Exclusive enteral feeding as primary therapy for Crohn's disease in Australian children and adolescents: a feasible and effective approach. J Gastroenterol Hepatol21:1609–1614 [CrossRef][PubMed]
    [Google Scholar]
  8. den Besten G., van Eunen K., Groen A. K., Venema K., Reijngoud D. J., Bakker B. M.. 2013; The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res54:2325–2340 [CrossRef][PubMed]
    [Google Scholar]
  9. Deshpande N. P., Kaakoush N. O., Wilkins M. R., Mitchell H. M.. 2013; Comparative genomics of Campylobacter concisus isolates reveals genetic diversity and provides insights into disease association. BMC Genomics14:585 [CrossRef][PubMed]
    [Google Scholar]
  10. Griffiths R. I., Whiteley A. S., O'Donnell A. G., Bailey M. J.. 2000; Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol66:5488–5491 [CrossRef][PubMed]
    [Google Scholar]
  11. IBD Working Group of the European Society for Paediatric Gastroenterology, Hepatology and Nutrition 2005; Inflammatory bowel disease in children and adolescents: recommendations for diagnosis: the Porto criteria. J Pediatr Gastroenterol Nutr41:1–7[PubMed][CrossRef]
    [Google Scholar]
  12. Hyams J. S., Mandel F., Ferry G. D., Gryboski J. D., Kibort P. M., Kirschner B. S., Griffiths A. M., Katz A. J., Boyle J. T.. 1992; Relationship of common laboratory parameters to the activity of Crohn's disease in children. J Pediatr Gastroenterol Nutr14:216–222 [CrossRef][PubMed]
    [Google Scholar]
  13. Kaakoush N. O., Deshpande N. P., Wilkins M. R., Tan C. G., Burgos-Portugal J. A., Raftery M. J., Day A. S., Lemberg D. A., Mitchell H.. 2011; The pathogenic potential of Campylobacter concisus strains associated with chronic intestinal diseases. PLoS One6:e29045 [CrossRef][PubMed]
    [Google Scholar]
  14. Kaakoush N. O., Mitchell H. M.. 2012; Campylobacter concisus: a new player in intestinal disease. Front Cell Infect Microbiol2:4 [CrossRef][PubMed]
    [Google Scholar]
  15. Kaakoush N. O., Castano-Rodriguez N., Day A. S., Lemberg D. A., Leach S. T., Mitchell H. M.. 2014a; Campylobacter concisus and exotoxin 9 levels in paediatric patients with Crohn's disease and their association with the intestinal microbiota. J Med Microbiol63:99–105 [CrossRef]
    [Google Scholar]
  16. Kaakoush N. O., Mitchell H. M., Man S. M.. 2014b; Role of emerging Campylobacter species in inflammatory bowel diseases. Inflamm Bowel Dis20:2189–2197 [CrossRef]
    [Google Scholar]
  17. Kaakoush N. O., Sodhi N., Chenu J. W., Cox J. M., Riordan S. M., Mitchell H. M.. 2014c; The interplay between Campylobacter and Helicobacter species and other gastrointestinal microbiota of commercial broiler chickens. Gut Pathogens6:18 [CrossRef]
    [Google Scholar]
  18. Kaakoush N. O., Castano-Rodriguez N., Day A. S., Lemberg D. A., Leach S. T., Mitchell H. M.. 2015a; Faecal levels of zonula occludens toxin in paediatric patients with Crohn's disease and their association with the intestinal microbiota. J Med Microbiol64:303–306 [CrossRef]
    [Google Scholar]
  19. Kaakoush N. O., Castaño-Rodríguez N., Man S. M., Mitchell H. M.. 2015b; Is Campylobacter to esophageal adenocarcinoma as Helicobacter is to gastric adenocarcinoma?. Trends Microbiol23:455–462 [CrossRef]
    [Google Scholar]
  20. Kaakoush N. O., Castaño-Rodríguez N., Mitchell H. M., Man S. M.. 2015c; Global epidemiology of Campylobacter infection. Clin Microbiol28:687–720 [CrossRef]
    [Google Scholar]
  21. Kaakoush N. O., Day A. S., Leach S. T., Lemberg D. A., Nielsen S., Mitchell H. M.. 2015d; Effect of exclusive enteral nutrition on the microbiota of children with newly diagnosed Crohn’s disease. Clin Transl Gastroenterol6:e71 [CrossRef]
    [Google Scholar]
  22. Lastovica A. J.. 2009; Clinical relevance of Campylobacter concisus isolated from pediatric patients. J Clin Microbiol47:2360 [CrossRef][PubMed]
    [Google Scholar]
  23. Le M. T., Porcelli I., Weight C. M., Gaskin D. J. H., Carding S. R., van Vliet A. H. M.. 2012; Acid-shock of Campylobacter jejuni induces flagellar gene expression and host cell invasion. Eur J Microbiol Immunol2:12–19 [CrossRef]
    [Google Scholar]
  24. Lynch O. A., Cagney C., McDowell D. A., Duffy G.. 2011; Occurrence of fastidious Campylobacter spp. in fresh meat and poultry using an adapted cultural protocol. Int J Food Microbiol150:171–177 [CrossRef][PubMed]
    [Google Scholar]
  25. Man S. M., Kaakoush N. O., Leach S. T., Nahidi L., Lu H. K., Norman J., Day A. S., Zhang L., Mitchell H. M.. 2010; Host attachment, invasion, and stimulation of proinflammatory cytokines by Campylobacter concisus and other non-Campylobacter jejuni Campylobacter species. J Infect Dis202:1855–1865 [CrossRef][PubMed]
    [Google Scholar]
  26. Nielsen H. L., Ejlertsen T., Engberg J., Nielsen H.. 2013; High incidence of Campylobacter concisus in gastroenteritis in North Jutland, Denmark: a population-based study. Clin Microbiol Infect19:445–450 [CrossRef][PubMed]
    [Google Scholar]
  27. Nielsen H. L., Engberg J., Ejlertsen T., Nielsen H.. 2014; Psychometric scores and persistence of irritable bowel after Campylobacter concisus infection. Scand J Gastroenterol49:545–551 [CrossRef][PubMed]
    [Google Scholar]
  28. Shimotoyodome A., Meguro S., Hase T., Tokimitsu I., Sakata T.. 2000; Short chain fatty acids but not lactate or succinate stimulate mucus release in the rat colon. Comp Biochem Physiol A Mol Integr Physiol125:525–531 [CrossRef][PubMed]
    [Google Scholar]
  29. Simpson H. L., Campbell B. J.. 2015; Dietary fibre–microbiota interactions. Aliment Pharmacol Ther42:158–179 [CrossRef][PubMed]
    [Google Scholar]
  30. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S.. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol28:2731–2739 [CrossRef][PubMed]
    [Google Scholar]
  31. von Rosenvinge E. C., Song Y., White J. R., Maddox C., Blanchard T., Fricke W. F.. 2013; Immune status, antibiotic medication and pH are associated with changes in the stomach fluid microbiota. ISME J7:1354–1366 [CrossRef][PubMed]
    [Google Scholar]
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