Bacteria-derived long chain fatty acid exhibits anti-inflammatory properties in colitis (original) (raw)

Bacteria-derived long chain fatty acid exhibits anti-inflammatory properties in colitis

Julien Pujo1,2,
Camille Petitfils1,
Pauline Le Faouder3,
Venessa Eeckhaut4,
Gaelle Payros1,
Sarah Maurel1,
Teresa Perez-Berezo1,
Matthias Van Hul5,
Frederick Barreau1,
Catherine Blanpied1,
Stephane Chavanas6,
Filip Van Immerseel4,
Justine Bertrand-Michel3,
Eric Oswald1,7,
http://orcid.org/0000-0001-5213-5378Claude Knauf1,8,
Gilles Dietrich1,
http://orcid.org/0000-0003-2040-2448Patrice D Cani5,8,
http://orcid.org/0000-0002-1552-7812Nicolas Cenac1
1IRSD, INSERM, INRA, INP-ENVT, Toulouse University 3 Paul Sabatier, Toulouse, France
2Farncombe Family Digestive Health Institute, McMaster University Faculty of Health Sciences, Hamilton, Ontario, Canada
3MetaToulLipidomics Facility, INSERM UMR1048, Toulouse, France
4Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium
5Walloon Excellence in Life Sciences and Biotechnology (WELBIO), Louvain Drug Research Institute, Metabolism and Nutrition Research Group, UCLouvain, Université catholique de Louvain, Brussels, Belgium
6Centre for Pathophysiology Toulouse-Purpan (CPTP), INSERM, CNRS, University of Toulouse, Toulouse, France
7Service de bactériologie-hygiène, CHU Toulouse, Hôpital Purpan, Toulouse, France
8NeuroMicrobiota, European Associated Laboratory (EAL), INSERM/UCLouvain, Toulouse, Brussels, France, Belgium
Correspondence to Dr Nicolas Cenac, UMR1220, IRSD, INSERM, Toulouse, Occitanie, France; nicolas.cenac{at}inserm.fr

Abstract

Objective Data from clinical research suggest that certain probiotic bacterial strains have the potential to modulate colonic inflammation. Nonetheless, these data differ between studies due to the probiotic bacterial strains used and the poor knowledge of their mechanisms of action.

Design By mass-spectrometry, we identified and quantified free long chain fatty acids (LCFAs) in probiotics and assessed the effect of one of them in mouse colitis.

Results Among all the LCFAs quantified by mass spectrometry in Escherichia coli Nissle 1917 (EcN), a probiotic used for the treatment of multiple intestinal disorders, the concentration of 3-hydroxyoctadecaenoic acid (C18-3OH) was increased in EcN compared with other E. coli strains tested. Oral administration of C18-3OH decreased colitis induced by dextran sulfate sodium in mice. To determine whether other bacteria composing the microbiota are able to produce C18-3OH, we targeted the gut microbiota of mice with prebiotic fructooligosaccharides (FOS). The anti-inflammatory properties of FOS were associated with an increase in colonic C18-3OH concentration. Microbiota analyses revealed that the concentration of C18-3OH was correlated with an increase in the abundance in Allobaculum, Holdemanella and Parabacteroides. In culture, Holdemanella biformis produced high concentration of C18-3OH. Finally, using TR-FRET binding assay and gene expression analysis, we demonstrated that the C18-3OH is an agonist of peroxisome proliferator activated receptor gamma.

Conclusion The production of C18-3OH by bacteria could be one of the mechanisms implicated in the anti-inflammatory properties of probiotics. The production of LCFA-3OH by bacteria could be implicated in the microbiota/host interactions.

enteric bacterial microflora
probiotics
lipids
experimental colitis
PPAR gamma

Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information.

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