Motility and biofilm formation of the emerging gastrointestinal pathogen Campylobacter concisus differs under microaerophilic and anaerobic environments.

Sandra Ovesen, Juliana Durack, Karina Frahm Kirk, Hans Linde Nielsen, Henrik Nielsen, Susan V Lynch
Author Information
  1. Sandra Ovesen: a Department of Medicine, Division of Gastroenterology , University of California San Francisco , San Francisco , CA , USA.
  2. Juliana Durack: a Department of Medicine, Division of Gastroenterology , University of California San Francisco , San Francisco , CA , USA.
  3. Karina Frahm Kirk: b Department of Infectious Diseases , Aalborg University Hospital , Aalborg , Denmark.
  4. Hans Linde Nielsen: c Department of Clinical Microbiology , Aalborg University Hospital , Aalborg , Denmark.
  5. Henrik Nielsen: b Department of Infectious Diseases , Aalborg University Hospital , Aalborg , Denmark.
  6. Susan V Lynch: a Department of Medicine, Division of Gastroenterology , University of California San Francisco , San Francisco , CA , USA.

Abstract

Campylobacter concisus has been isolated from patients with gastroenteritis and inflammatory bowel disease (IBD), as well as healthy subjects. While strain differences may plausibly explain virulence differentials, an alternative hypothesis posits that the pathogenic potential of this species may depend on altered ecosystem conditions in the inflamed gut. One potential difference is oxygen availability, which is frequently increased under conditions of inflammation and is known to regulate bacterial virulence. Hence, we hypothesized that oxygen influences C. concisus physiology. We therefore characterized the effect of microaerophilic or anaerobic environments on C. concisus motility and biofilm formation, two important determinants of host colonization and dissemination. C. concisus isolates (n = 46) sourced from saliva, gut mucosal biopsies and feces of patients with IBD (n = 23), gastroenteritis (n = 8) and healthy subjects (n = 13), were used for this study. Capacity to form biofilms was determined using crystal violet assay, while assessment of dispersion through soft agar permitted motility to be assessed. No association existed between GI disease and either motility or biofilm forming capacity. Oral isolates exhibited significantly greater capacity for biofilm formation compared to fecal isolates (p<0.03), and showed a strong negative correlation between motility and biofilm formation (r = -0.7; p = 0.01). Motility significantly increased when strains were cultured under microaerophilic compared to anaerobic conditions (p<0.001). Increased biofilm formation under microaerophillic conditions was also observed for a subset of isolates. Hence, differences in oxygen availability appear to influence key physiological aspects of the opportunistic gastrointestinal pathogen C. concisus.

Keywords

References

  1. Trends Microbiol. 2002 Apr;10(4):155-9 [PMID: 11912013]
  2. Scand J Infect Dis. 2002;34(4):248-52 [PMID: 12064685]
  3. J Med Microbiol. 2005 Sep;54(Pt 9):889-95 [PMID: 16091443]
  4. J Clin Microbiol. 2005 Oct;43(10):5091-6 [PMID: 16207968]
  5. J Mol Biol. 1991 Jun 5;219(3):443-50 [PMID: 1646892]
  6. Appl Environ Microbiol. 2007 Mar;73(6):1908-13 [PMID: 17259368]
  7. Annu Rev Med. 2008;59:415-28 [PMID: 17937586]
  8. Food Microbiol. 2009 Feb;26(1):44-51 [PMID: 19028304]
  9. Gastroenterology. 2009 Aug;137(2):495-501 [PMID: 19361507]
  10. Arch Microbiol. 2010 Jul;192(7):507-20 [PMID: 20411245]
  11. Int J Food Microbiol. 2010 Oct 15;143(3):118-24 [PMID: 20805009]
  12. J Infect Dis. 2010 Dec 15;202(12):1855-65 [PMID: 21050118]
  13. Cell Microbiol. 2011 Feb;13(2):171-6 [PMID: 21166974]
  14. J Vis Exp. 2011 Jan 30;(47):null [PMID: 21307833]
  15. Age (Dordr). 2012 Feb;34(1):247-67 [PMID: 21347607]
  16. BMC Microbiol. 2011 Mar 15;11:53 [PMID: 21406111]
  17. PLoS One. 2011;6(8):e23858 [PMID: 21887334]
  18. PLoS Pathog. 2011 Sep;7(9):e1002253 [PMID: 21949654]
  19. PLoS One. 2011;6(9):e25417 [PMID: 21966525]
  20. Gut Pathog. 2011 Oct 13;3:15 [PMID: 21992484]
  21. PLoS One. 2011;6(12):e29045 [PMID: 22194985]
  22. Clin Microbiol Infect. 2013 May;19(5):445-50 [PMID: 22512739]
  23. Curr Gastroenterol Rep. 2012 Oct;14(5):395-405 [PMID: 22864805]
  24. Gut Pathog. 2012 Dec 14;4(1):22 [PMID: 23241133]
  25. Scand J Gastroenterol. 2013 May;48(5):633-5 [PMID: 23448294]
  26. ISME J. 2013 Jul;7(7):1354-66 [PMID: 23466701]
  27. FEMS Microbiol Rev. 2013 Nov;37(6):849-71 [PMID: 23480406]
  28. ISME J. 2013 Jul;7(7):1256-61 [PMID: 23677008]
  29. Inflamm Bowel Dis. 2014 Nov;20(11):2189-97 [PMID: 24874462]
  30. Int J Microbiol. 2014;2014:476047 [PMID: 25214843]
  31. Appl Environ Microbiol. 2014 Nov;80(22):7096-106 [PMID: 25261508]
  32. Gut Pathog. 2014 Sep 09;6:38 [PMID: 25349633]
  33. Microb Ecol Health Dis. 2015 Feb 02;26:26050 [PMID: 25651996]
  34. Trends Microbiol. 2015 Aug;23(8):455-62 [PMID: 25937501]
  35. Clin Microbiol Rev. 2015 Jul;28(3):687-720 [PMID: 26062576]
  36. World J Gastroenterol. 2015 Aug 21;21(31):9239-44 [PMID: 26309350]
  37. Gut Pathog. 2016 Jun 01;8:27 [PMID: 27252786]
  38. Virulence. 2016 Oct 2;7(7):846-51 [PMID: 27268722]
  39. MBio. 2016 Sep 13;7(5): [PMID: 27624126]
  40. Free Radic Biol Med. 2017 Apr;105:93-101 [PMID: 27677568]
  41. Gut Pathog. 2016 Sep 22;8:44 [PMID: 27688814]
  42. APMIS. 2017 Mar;125(3):230-235 [PMID: 28116789]
  43. Curr Opin Microbiol. 2017 Feb;35:64-69 [PMID: 28189956]
  44. Sci Rep. 2018 Jan 30;8(1):1902 [PMID: 29382867]
  45. J Bacteriol. 1993 Jul;175(14):4448-55 [PMID: 8331072]
  46. Mol Microbiol. 1996 Apr;20(2):351-60 [PMID: 8733233]
  47. Appl Environ Microbiol. 1998 Oct;64(10):3917-22 [PMID: 9758819]

MeSH Term

Adolescent
Adult
Aerobiosis
Aged
Anaerobiosis
Biofilms
Campylobacter
Campylobacter Infections
Female
Gastroenteritis
Humans
Inflammatory Bowel Diseases
Male
Middle Aged
Oxygen
Young Adult

Chemicals

Oxygen

Word Cloud

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