Journal Article

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

Maurel, Sarah, Dietrich, Gilles, Knauf, Claude, Oswald, Eric, Blanpied, Catherine, Pujo, Julien, Van Immerseel, Filip, Cani, Patrice D, Le Faouder, Pauline, Eeckhaut, Venessa, Cenac, Nicolas, Perez-Berezo, Teresa, Chavanas, Stephane, Barreau, Frederick, Van Hul, Matthias, Bertrand-Michel, Justine, Petitfils, Camille, Payros, Gaelle

2021

Overview

ObjectiveData 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.DesignBy 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.ResultsAmong 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.ConclusionThe 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.

• Publisher: BMJ Publishing Group Ltd and British Society of Gastroenterology,BMJ Publishing Group LTD,BMJ Publishing Group
• Subject: Animals / Anti-inflammatory agents / Antibiotics / Bacteria / Bacteriology / Bacteroidetes / Biochemistry, Molecular Biology / Caco-2 Cells / Carbon / Cell Membrane Permeability / Chemokine CXCL1 - genetics / Chromatography / Colitis / Colitis - chemically induced / Colitis - drug therapy / Colitis - metabolism / Dextran / Dextran Sulfate / Diarrhea / E coli / enteric bacterial microflora / Epithelial Cells - physiology / Escherichia coli / Escherichia coli - metabolism / experimental colitis / Experiments / Fatty acids / Firmicutes - metabolism / Fluorescence resonance energy transfer / Fourier transforms / Fructooligosaccharides / Gastrointestinal Microbiome - physiology / Gene expression / Gene Expression - drug effects / Gut microbiota / Human health and pathology / Humans / Inflammation / Inflammatory bowel disease / Interleukin-1beta - genetics / Intestinal microflora / Intestinal Mucosa - metabolism / Intestine / Life Sciences / lipids / Mass Spectrometry / Mass spectroscopy / Metabolites / Mice / Microbiology and Parasitology / Microbiota / Oligosaccharides - pharmacology / Oral administration / Pancreatitis-Associated Proteins - genetics / Pathogens / Permeability / Peyer's Patches / Phylogenetics / PPAR gamma / PPAR gamma - genetics / PPAR gamma - metabolism / Prebiotics / Probiotics / Probiotics - chemistry / Proteins / Stearates - analysis / Stearates - metabolism / Stearates - therapeutic use / Strains (organisms) / Tissues and Organs / Zonula Occludens-1 Protein - genetics