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. 2024 Jun 29;24(1):233.
doi: 10.1186/s12866-024-03368-4.

Taxonomic and phenotypic analysis of bifidobacteria isolated from IBD patients as potential probiotic strains

Sabine Bosselaar  1   2 , Lucile Dhelin  3 , Ellena Dautel  3 , Marie Titecat  4 , Stéphanie Duthoy  3 , Marie Stelmaszczyk  3 , Nathan Delory  3 , Madeleine De Sousa Violante  3 , François Machuron  3 , Hassina Ait-Abderrahim  3 , Pierre Desreumaux  4   5 , Benoit Foligné  4 , Céline Monnet  3
Affiliations

Taxonomic and phenotypic analysis of bifidobacteria isolated from IBD patients as potential probiotic strains

Sabine Bosselaar et al. BMC Microbiol. .

Abstract

Background: Inflammatory Bowel Diseases (IBD) are a major public health issue with unclear aetiology. Changes in the composition and functionality of the intestinal microbiota are associated with these pathologies, including the depletion of strict anaerobes such as Feacalibacterium prausnitzii. Less evidence is observed for depletion in other anaerobes, among which bifidobacteria. This study characterized the taxonomic and functional diversity of bifidobacteria isolated from the human intestinal microbiota in active and non-active IBD patients by a culturomics approach and evaluated if these bifidobacteria might be used as probiotics for gut health.

Results: A total of 341 bifidobacteria were isolated from the intestinal microbiota of IBD patients (52 Crohn's disease and 26 ulcerative colitis patients), with a high proportion of Bifidobacterium dentium strains (28% of isolated bifidobacteria). In ulcerative colitis, the major species identified was B. dentium (39% of isolated bifidobacteria), in active and non-active ulcerative colitis. In Crohn's disease, B. adolescentis was the major species isolated from non-active patients (40%), while similar amounts of B. dentium and B. adolescentis were found in active Crohn's disease patients. The relative abundance of B. dentium was increased with age, both in Crohn's disease and ulcerative colitis and active and non-active IBD patients. Antibacterial capacities of bifidobacteria isolated from non-active ulcerative colitis against Escherichia coli LF82 and Salmonella enterica ATCC 14028 were observed more often compared to strains isolated from active ulcerative colitis. Finally, B. longum were retained as strains with the highest probiotic potential as they were the major strains presenting exopolysaccharide synthesis, antibacterial activity, and anti-inflammatory capacities. Antimicrobial activity and EPS synthesis were further correlated to the presence of antimicrobial and EPS gene clusters by in silico analysis.

Conclusions: Different bifidobacterial taxonomic profiles were identified in the microbiota of IBD patients. The most abundant species were B. dentium, mainly associated to the microbiota of ulcerative colitis patients and B. adolescentis, in the intestinal microbiota of Crohn's disease patients. Additionally, the relative abundance of B. dentium significantly increased with age. Furthermore, this study evidenced that bifidobacteria with probiotic potential (antipathogenic activity, exopolysaccharide production and anti-inflammatory activity), especially B. longum strains, can be isolated from the intestinal microbiota of both active and non-active Crohn's disease and ulcerative colitis patients.

Keywords: Bifidobacteria; Culturomics; Functional characterization; Inflammatory Bowel Diseases; Microbiota.

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Conflict of interest statement

This study was a collaboration between Lesaffre International and Infinite (Inserm, CHU Lille, U1286, France). SB, LD, ED, SD, MS, ND, MDSV, FM, HAA and CM are employees of Lesaffre International, who funded this study. P.D. reports personal fees from Lesaffre and several pharmaceutical companies, Abbott, Amgen, Biocodex, Biofortis, Biogen, Biokuris, Ferring, Fresenius, Janssen Kitozyme, MSD, Norgine, Pfizer, Sandoz, Shire, Takeda, Tillotts, and UCB, outside of the submitted work. Other authors declared no competing interests.

Figures

Fig. 1
Fig. 1
Bacterial enumeration of fecal samples on Columbia Beerens medium (Bifidobacteriaceae enrichment) and Columbia blood agar (Total bacteria) grouped by pathology and disease activity. Boxplots represent median (solid line), first and third quartile (lower and upper boundaries), lower and upper limits (whiskers, defined by 1.5* inter quartile range) and outliers (dotpoints). Wilcoxon test p-values: *: 0.01–0.05; **: 0.001–0.01; ***: < 0.001; ns: > 0.05. N: number of samples per group
Fig. 2
Fig. 2
Taxonomic species identification of the 341 bifidobacteria strains isolated from 78 IBD patients (N = 52 Crohn’s disease patients + N = 26 Ulcerative colitis patients). Ratios are presented as relative abundance of bifidobacteria isolated (absolute number of bifidobacteria strains isolated)
Fig. 3
Fig. 3
Characterization of the bifidobacteria profile in intestinal microbiota of IBD patients by (A) pathology or (B) disease activity. Ratios are presented as relative proportion of bifidobacteria isolated (absolute number of strains isolated). Ratios were not displayed for species with relative abundance ≤ 5%. Chi2 test p-values: *: 0.01–0.05; **: 0.001–0.01; ***: < 0.001; ns: > 0.05. N: number of samples from which strains were isolated. n: number of strains isolated
Fig. 4
Fig. 4
Characterization of the bifidobacteria profile in intestinal microbiota of IBD patients by age (A) for all patients, (B) per pathology and (C) per disease activity. Ratios are presented as relative proportion of bifidobacteria isolated (absolute number of bifidobacteria strains isolated). Ratios were not displayed for species with relative abundance ≤ 5%. N: number of samples from which strains were isolated. n: number of strains isolated. Chi.2 test p-values: *: 0.01–0.05; **: 0.001–0.01; ***: < 0.001; ns: > 0.05
Fig. 5
Fig. 5
Growth characterization of bifidobacteria in (A) anaerobic and (B) microaerophilic (under 5% 02) conditions. A Growth parameters were not determined for strains with Max OD600nm < 0.2 or that did not reach end of exponential phase after 48h. Boxplots represent median (solid line), first and third quartile (lower and upper boundaries), lower and upper limits (whiskers, defined by 1.5* inter quartile range) and outliers (dotpoints). (B) Not determined: strains that did not present growth in control condition (anaerobic) to calculate microaerophilic growth ratio
Fig. 6
Fig. 6
EPS production on 20g/L glucose MRS agar plates (A) per bifidobacterial species and (B) according to strain origin (pathology and disease activity). Chi.2 test p-values: *: 0.01–0.05; **: 0.001–0.01; ***: < 0.001; ns: > 0.05
Fig. 7
Fig. 7
Inhibition of E. coli LF82 and Salmonella enterica ATCC 14028 by bifidobacteria. A Inhibition profiles by bifidobacteria per species and per pathogen tested. B Global inhibition profiles by bifidobacteria species (number of pathogens inhibited). C Inhibition profiles by bifidobacteria per pathogen tested according to isolation origin (pathology and disease activity). D Global inhibition profiles according to isolation origin (pathology and disease activity). Chi2 test p-values: *: 0.01–0.05; **: 0.001–0.01; ***: < 0.001; ns: > 0.05. n: number of strains. Not determined: insufficient growth of bifidobacterial strain in experiment conditions
Fig. 8
Fig. 8
Biosynthetic gene clusters identified in bifidobacteria genomes by combined analysis with antiSMASH and BAGEL4
Fig. 9
Fig. 9
Immunomodulatory activity of bifidobacteria by inhibition of IL8 secretion of HT29 cells. (A) Immunomodulatory profile of all bifidobacteria per species. (B) Immunomodulatory profile of B. longum according to disease activity. Chi2 test p-values: *: 0.01–0.05; **: 0.001–0.01; ***: < 0.001; ns: > 0.05. n: number of strains
Fig. 10
Fig. 10
Summary of bifidobacteria characterization in IBD patients
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