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Effect of supplementation of a dairy-originated probiotic bacterium, Propionibacterium freudenreichii subsp. freudenreichii, on the cecal microbiome of turkeys challenged with multidrug-resistant Salmonella Heidelberg.

ABSTRACT: A dairy-originated probiotic bacterium, Propionibacterium freudenreichii subsp. freudenreichii B3523 (PF) was found to be effective in reducing multidrug-resistant Salmonella Heidelberg (MDR SH) colonization in turkey poults (2-week-old) and growing (7-week-old) and finishing (12-week-old) turkeys. In this study, we explored the potential for microbiome modulation in the cecum of turkeys of different age groups due to PF supplementation in conjunction with MDR SH challenge. One-day-old commercial turkey poults were allocated to 3 treatment groups: negative control (N; turkeys without PF supplementation or SH challenge), SH control (S; turkeys challenged with SH without PF supplementation), and test group (P; turkeys supplemented with PF and challenged with SH). Turkeys were supplemented with 10¹⁰ CFU PF in 5-gallon (18.9 L) water until 7 or 12 week of age. At the 6th or 11^th wk, turkeys were challenged with SH at 10⁶ and 10⁸ CFU/bird by crop gavage, respectively. After 2 and 7 d of challenge (2-d postinoculation [PI] and 7-d PI, respectively), cecal samples were collected and microbiome analysis was conducted using Illumina MiSeq. The experiments were repeated twice with 8 and 10 turkeys/group for 7- and 12-wk studies, respectively. Results indicated that the species richness and abundance (Shannon diversity index) was similar among the treatment groups. However, treatments caused apparent clustering of the samples among each other (P < 0.05). Firmicutes was the predominant phylum in the growing and finishing turkey cecum which was evenly distributed among the treatments except on wk 12 where the relative abundance of Firmicutes was significantly higher in P than in N (P = 0.02). The MDR SH challenge resulted in modulation of microflora such as Streptococcus, Gordonibacter, and Turicibacter (P < 0.05) in the S groups compared with the P and N groups, known to be associated with inflammatory responses in birds and mammals. The supplementation of PF increased the relative abundance of carbohydrate-fermenting and short-chain fatty acid-producing genera in the P group compared with the S group (P < 0.05). Moreover, the results revealed that PF supplementation potentially modulated the beneficial microbiota in the P group, which could mitigate SH carriage in turkeys.

SUBMITTER: Nair DVT

PROVIDER: S-EPMC7772705 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Effect of supplementation of a dairy-originated probiotic bacterium, Propionibacterium freudenreichii subsp. freudenreichii, on the cecal microbiome of turkeys challenged with multidrug-resistant Salmonella Heidelberg.

Nair D V T DVT Johnson T J TJ Noll S L SL Kollanoor Johny A A

Poultry science 20201012 1

A dairy-originated probiotic bacterium, Propionibacterium freudenreichii subsp. freudenreichii B3523 (PF) was found to be effective in reducing multidrug-resistant Salmonella Heidelberg (MDR SH) colonization in turkey poults (2-week-old) and growing (7-week-old) and finishing (12-week-old) turkeys. In this study, we explored the potential for microbiome modulation in the cecum of turkeys of different age groups due to PF supplementation in conjunction with MDR SH challenge. One-day-old commercia ...[more]

PMID: 33357692

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Project description:BACKGROUND: Propionibacterium freudenreichii is essential as a ripening culture in Swiss-type cheeses and is also considered for its probiotic use. This species exhibits slow growth, low nutritional requirements, and hardiness in many habitats. It belongs to the taxonomic group of dairy propionibacteria, in contrast to the cutaneous species P. acnes. The genome of the type strain, P. freudenreichii subsp. shermanii CIRM-BIA1 (CIP 103027(T)), was sequenced with an 11-fold coverage. METHODOLOGY/PRINCIPAL FINDINGS: The circular chromosome of 2.7 Mb of the CIRM-BIA1 strain has a GC-content of 67% and contains 22 different insertion sequences (3.5% of the genome in base pairs). Using a proteomic approach, 490 of the 2439 predicted proteins were confirmed. The annotation revealed the genetic basis for the hardiness of P. freudenreichii, as the bacterium possesses a complete enzymatic arsenal for de novo biosynthesis of aminoacids and vitamins (except panthotenate and biotin) as well as sequences involved in metabolism of various carbon sources, immunity against phages, duplicated chaperone genes and, interestingly, genes involved in the management of polyphosphate, glycogen and trehalose storage. The complete biosynthesis pathway for a bifidogenic compound is described, as well as a high number of surface proteins involved in interactions with the host and present in other probiotic bacteria. By comparative genomics, no pathogenicity factors found in P. acnes or in other pathogenic microbial species were identified in P. freudenreichii, which is consistent with the Generally Recognized As Safe and Qualified Presumption of Safety status of P. freudenreichii. Various pathways for formation of cheese flavor compounds were identified: the Wood-Werkman cycle for propionic acid formation, amino acid degradation pathways resulting in the formation of volatile branched chain fatty acids, and esterases involved in the formation of free fatty acids and esters. CONCLUSIONS/SIGNIFICANCE: With the exception of its ability to degrade lactose, P. freudenreichii seems poorly adapted to dairy niches. This genome annotation opens up new prospects for the understanding of the P. freudenreichii probiotic activity.

Project description:BACKGROUND: Propionibacterium freudenreichii is a food grade bacterium consumed both in cheeses and in probiotic preparations. Its promising probiotic potential, relying largely on the active release of beneficial metabolites within the gut as well as the expression of key surface proteins involved in immunomodulation, deserves to be explored more deeply. Adaptation to the colon environment is requisite for the active release of propionibacterial beneficial metabolites and constitutes a bottleneck for metabolic activity in vivo. Mechanisms allowing P. freudenreichii to adapt to digestive stresses have been only studied in vitro so far. Our aim was therefore to study P. freudenreichii metabolic adaptation to intra-colonic conditions in situ. RESULTS: We maintained a pure culture of the type strain P. freudenreichii CIRM BIA 1, contained in a dialysis bag, within the colon of vigilant piglets during 24 hours. A transcriptomic analysis compared gene expression to identify the metabolic pathways induced by this environment, versus control cultures maintained in spent culture medium.We observed drastic changes in the catabolism of sugars and amino-acids. Glycolysis, the Wood-Werkman cycle and the oxidative phosphorylation pathways were down-regulated but induction of specific carbohydrate catabolisms and alternative pathways were induced to produce NADH, NADPH, ATP and precursors (utilizing of propanediol, gluconate, lactate, purine and pyrimidine and amino-acids). Genes involved in stress response were down-regulated and genes specifically expressed during cell division were induced, suggesting that P. freudenreichii adapted its metabolism to the conditions encountered in the colon. CONCLUSIONS: This study constitutes the first molecular demonstration of P. freudenreichii activity and physiological adaptation in vivo within the colon. Our data are likely specific to our pig microbiota composition but opens an avenue towards understanding probiotic action within the gut in further studies comparing bacterial adaptation to different microbiota.

Project description:Propionibacterium freudenreichii is a beneficial Gram-positive bacterium, traditionally used as a cheese-ripening starter, and currently considered as an emerging probiotic. As an example, the P. freudenreichii CIRM-BIA 129 strain recently revealed promising immunomodulatory properties. Its consumption accordingly exerts healing effects in different animal models of colitis, suggesting a potent role in the context of inflammatory bowel diseases. This anti-inflammatory effect depends on surface layer proteins (SLPs). SLPs may be involved in key functions in probiotics, such as persistence within the gut, adhesion to host cells and mucus, or immunomodulation. Several SLPs coexist in P. freudenreichii CIRM-BIA 129 and mediate immunomodulation and adhesion. A mutant P. freudenreichii CIRM-BIA 129?slpB (CB129?slpB) strain was shown to exhibit decreased adhesion to intestinal epithelial cells. In the present study, we thoroughly analyzed the impact of this mutation on cellular properties. Firstly, we investigated alterations of surface properties in CB129?slpB. Surface extractable proteins, surface charges (?-potential) and surface hydrophobicity were affected by the mutation. Whole-cell proteomics, using high definition mass spectrometry, identified 1,288 quantifiable proteins in the wild-type strain, i.e., 53% of the theoretical proteome predicted according to P. freudenreichii CIRM-BIA 129 genome sequence. In the mutant strain, we detected 1,252 proteins, including 1,227 proteins in common with the wild-type strain. Comparative quantitative analysis revealed 97 proteins with significant differences between wild-type and mutant strains. These proteins are involved in various cellular process like signaling, metabolism, and DNA repair and replication. Finally, in silico analysis predicted that slpB gene is not part of an operon, thus not affecting the downstream genes after gene knockout. This study, in accordance with the various roles attributed in the literature to SLPs, revealed a pleiotropic effect of a single slpB mutation, in the probiotic P. freudenreichii. This suggests that SlpB may be at a central node of cellular processes and confirms that both nature and amount of SLPs, which are highly variable within the P. freudenreichii species, determine the probiotic abilities of strains.

Dataset Information

Effect of supplementation of a dairy-originated probiotic bacterium, Propionibacterium freudenreichii subsp. freudenreichii, on the cecal microbiome of turkeys challenged with multidrug-resistant Salmonella Heidelberg.

Publications

Effect of supplementation of a dairy-originated probiotic bacterium, Propionibacterium freudenreichii subsp. freudenreichii, on the cecal microbiome of turkeys challenged with multidrug-resistant Salmonella Heidelberg.

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