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The Stressogenic Impact of Bacterial Secretomes Is Modulated by the Size of the Milk Fat Globule Used as a Substrate.

ABSTRACT: Milk fat globules (MFGs) are produced by mammary epithelial cells (MECs) and originate from intracellular lipid droplets with a wide size distribution. In the mammary gland and milk, bacteria can thrive on MFGs. Herein, we aimed to investigate whether the response of MECs to the bacterial secretome is dependent on the MFG size used as a substrate for the bacteria, and whether the response differs between pathogenic and commensal bacteria. We used secretomes from both Bacillus subtilis and E. coli. Proinflammatory gene expression in MECs was elevated by the bacteria secretomes from both bacteria sources, while higher expression was found in cells exposed to the secretome of bacteria grown on large MFGs. The secretome of B. subtilis reduced lipid droplet size in MECs. When the secretome originated from E. coli, lipid droplet size in MEC cytoplasm was elevated with a stronger response to the secretome from bacteria grown on large compared with small MFGs. These results indicate that MEC response to bacterial output is modulated by bacteria type and the size of MFGs used by the bacteria, which can modulate the stress response of the milk-producing cells, their lipid output, and consequently milk quality.

SUBMITTER: Tzirkel-Hancock N

PROVIDER: S-EPMC11312077 | biostudies-literature | 2024 Aug

REPOSITORIES: biostudies-literature

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The Stressogenic Impact of Bacterial Secretomes Is Modulated by the Size of the Milk Fat Globule Used as a Substrate.

Tzirkel-Hancock Noam N Raz Chen C Sharabi Lior L Argov-Argaman Nurit N

Foods (Basel, Switzerland) 20240801 15

Milk fat globules (MFGs) are produced by mammary epithelial cells (MECs) and originate from intracellular lipid droplets with a wide size distribution. In the mammary gland and milk, bacteria can thrive on MFGs. Herein, we aimed to investigate whether the response of MECs to the bacterial secretome is dependent on the MFG size used as a substrate for the bacteria, and whether the response differs between pathogenic and commensal bacteria. We used secretomes from both <i>Bacillus subtilis</i> and ...[more]

PMID: 39123620

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Project description:The aim of this study was to evaluate the effect of conjugated linoleic acid (CLA) on milk fat globule (MFG) size and the ruminal microbiome of goats. Twenty-four mid-lactation Saanen dairy goats weighing 49 ± 4.5 kg (168 ± 27 d in milk, 1.2 ± 0.1 kg milk/d, 2-3 years old) were randomly divided into four groups-a control (CON) group, which was fed a basal diet, and three CLA supplementation groups, in which 30 g CLA (low-dose group, L-CLA), 60 g CLA (medium-dose group, M-CLA), or 90 g CLA (high-dose group, H-CLA) was added to the basal diet daily. The experiment lasted for 21 days, during which time goat milk was collected for composition and MFG size analysis. On day 21 of feeding, ruminal fluid was collected from the CON and H-CLA groups for analysis of the changes in microorganismal abundance. The results showed that CLA supplementation did not affect milk production, milk protein, or lactose content in the dairy goats (p > 0.05), but significantly reduced the milk fat content (p < 0.01) compared with the CON group. The CLA supplementation significantly decreased the D[3,2] and D[4,3] of the MFGs in a dose-dependent manner (p < 0.01). Moreover, dietary CLA inclusion increased the proportion of small-sized MFGs and decreased that of large-sized ones. The results of 16S rRNA gene sequencing showed that CLA-induced milk fat depression in dairy goats was accompanied by significant changes in the relative abundance of ruminal bacterial populations, most of which belonged to the Firmicutes and Bacteroidetes phyla. The relative abundance of Rikenellaceae_RC9_gut_group and Prevolellaceae_UCG-003 in Bacteroidetes and UCG-002, Succiniclasticum, and norank_f__norank_o__Clostridia_vadinBB60_group in Firmicutes was significantly higher in the CON group than in the H-CLA group. In contrast, the relative abundance of norank_f__UCG-011, norank_f_Eubacterium_coprostanoligenes_group, unclassified_f__Lachnospiraceae, and UCG-001 in Firmicutes and norank_f__Muribaculaceae in Bacteroidetes was significantly higher in the H-CLA group than in the CON group. Correlation analysis showed that the milk fat content was negatively correlated with the relative abundance of some bacteria, including members of Firmicutes and Bacteroidetes. Similarly, MFG size (D[3,2] and D[4,3]) was negatively correlated with several members of Firmicutes and Bacteroidetes, including Lachnospiraceae, norank_f__UCG-011, UCG-001, norank_f__Eubacterium_coprostanoligenes_group (Firmicutes), and norank_f__Muribaculaceae (Bacteroidetes), while positively correlated with the relative abundance of some members of Firmicutes and Bacteroidetes, including Mycoplasma, Succiniclasticum, norank_f__norank_o__Clostridia_vadinBB60_group, UCG-002 (Firmicutes), and Rikenellaceae_RC9_gut_group (Bacteroidetes). Overall, our data indicated that CLA treatment affected milk fat content and MFG size in dairy goats, and these effects were correlated with the relative abundance of ruminal bacterial populations. These results provide the first evidence to explain the mechanism underlying diet-induced MFG from the perspective of the ruminal microbiome in dairy goats.

Project description:BackgroundProteins and lipids of milk fat globule membrane (MFGM) and probiotics are immunomodulatory. We hypothesized that Lactobacillus paracasei ssp. paracasei strain F19 (F19) would augment vaccine antibody and T helper 1 type immune responses whereas MFGM would produce an immune response closer to that of breastfed (BF) infants.ObjectiveTo compare the effects of supplementing formula with F19 or bovine MFGM on serum cytokine and vaccine responses of formula-fed (FF) and BF infants.DesignFF infants were randomized to formula with F19 (n = 195) or MFGM (n = 192), or standard formula (SF) (n = 194) from age 21±7 days until 4 months. A BF group served as reference (n = 208). We analyzed seven cytokines (n = 398) in serum at age 4 months using magnetic bead-based multiplex technology. Using ELISA, we analyzed anti-diphtheria IgG (n = 258) and anti-poliovirus IgG (n = 309) concentrations in serum before and after the second and third immunization, respectively.ResultsCompared with SF, the F19 group had greater IL-2 and lower IFN-γ concentrations (p<0.05, average effect size 0.14 and 0.39). Compared with BF, the F19 group had greater IL-2, IL-4 and IL-17A concentrations (p<0.05, average effect size 0.42, 0.34 and 0.26, respectively). The MFGM group had lower IL-2 and IL-17A concentrations compared with SF (p<0.05, average effect size 0.34 and 0.31). Cytokine concentrations were comparable among the MFGM and BF groups. Vaccine responses were comparable among the formula groups.ConclusionsContrary to previous studies F19 increased IL-2 and lowered IFN-γ production, suggesting that the response to probiotics differs across populations. The cytokine profile of the MFGM group approached that of BF infants, and may be associated with the previous finding that infectious outcomes for the MFGM group in this cohort were closer to those of BF infants, as opposed to the SF group. These immunomodulatory effects support future clinical evaluation of infant formula with F19 or MFGM.

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The Stressogenic Impact of Bacterial Secretomes Is Modulated by the Size of the Milk Fat Globule Used as a Substrate.

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The Stressogenic Impact of Bacterial Secretomes Is Modulated by the Size of the Milk Fat Globule Used as a Substrate.

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