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. 2024 Jul 11;12(7):1403.
doi: 10.3390/microorganisms12071403.

Fermented Purslane (Portulaca oleracea L.) Supplementation Enhances Growth and Immune Function Parallel to the Regulation of Gut Microbial Butyrate Production in Weaned Piglets

Lei Xu  1 , Ge Gao  1 , Zian Zhou  2 , Zixi Wei  1 , Wenjuan Sun  1 , Yanpin Li  1 , Xianren Jiang  1 , Jingang Gu  2 , Xilong Li  1 , Yu Pi  1
Affiliations

Fermented Purslane (Portulaca oleracea L.) Supplementation Enhances Growth and Immune Function Parallel to the Regulation of Gut Microbial Butyrate Production in Weaned Piglets

Lei Xu et al. Microorganisms. .

Abstract

Weaning is a challenging period for piglets, characterized by stress-related growth checks, compromised immunity, and gut dysbiosis. Purslane (Portulaca oleracea L.), known for its rich content of antioxidants, has potential as a functional feed ingredient. This study investigates the effects of feeding fermented purslane (FP) on the growth performance, immune function, intestinal microbiota, and metabolic profiles of weaned piglets. Forty-eight weaned piglets were randomly divided into two groups, with eight pens in each group and three pigs in each pen: a control diet (CON group) and a diet supplemented with 0.20% FP (FP group). The experiment lasted 28 days. The results show that FP supplementation did not affect the average daily feed intake (ADFI) but significantly increased the average daily gain (ADG) during the initial 14 days post-weaning. FP supplementation decreased diarrhea occurrence, with a pronounced reduction from days 10 to 13 (p < 0.05). Immunologically, the FP group had a trend towards reduced serum IgA levels on day 14 (p < 0.10). Importantly, the serum concentrations of the pro-inflammatory cytokine IL-6 were significantly reduced on both days 14 and 28 post-weaning. The antioxidative analysis showed increased serum superoxide dismutase (SOD) and decreased catalase (CAT) activities on day 14 (p < 0.05). In addition, FP supplementation significantly decreased serum diamine oxidase (DAO) activity and D-lactate levels by day 28, indicating a potential improvement in gut integrity. Fecal microbiota assessment demonstrated a distinctive clustering of microbial communities between the FP and CON groups, with an increase in the abundance of Clostridium_sensu_stricto_1, Tyzzerella, and Prevotellaceae_NK3B31_group and a decrease in Lactobacillus, Bacillus, and Subdoligranulum in the FP group (p < 0.05). Functional predictions suggested that the relative abundance of microbial butyrate synthesis enzymes (EC 2.7.2.7 and EC 2.3.1.19) was significantly enhanced by FP treatment. This modulation was further corroborated by elevated fecal butyrate levels (p < 0.05). In summary, dietary supplementation with FP promotes early-growth performance and has beneficial effects on immune function and intestinal health in weaned piglets. The enhancements may be attributed to distinct microbiota compositional changes and targeted modulation of microbial butyrate metabolism, which are crucial for piglet post-weaning adaptation and overall health.

Keywords: diarrhea; fermented purslane; immunoregulation; microbial butyrate synthesis; piglet.

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Conflict of interest statement

The authors declare that the research study was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.

Figures

Figure 1
Figure 1
Effects of dietary supplementation of FP on growth performance and diarrhea rate in weaning piglets (n = 8). (A) Average daily feed intake; (B) average daily weight gain; (C) F/G; (D) diarrhea incidence. CON, piglets that were fed a standard corn–soybean meal basal diet; FP, piglets that were fed a basal diet supplemented with 0.20% fermented purslane. All data are presented as means ± SEM. *, p < 0.05; **, p < 0.01.
Figure 2
Figure 2
Effects of dietary supplementation of FP on immune indicators in weaning piglets (n = 8). (A) Serum immunoglobulin levels; (B) serum cytokines level. IgA, immunoglobulin A; IgG, immunoglobulin G; IgM, immunoglobulin M; TNF-α, tumor necrosis factor-α; IL-6, interleukin 6; IL-1β, interleukin 1β; IL-10, interleukin 10; CON, piglets that were fed a standard corn–soybean meal basal diet; FP, piglets that were fed a basal diet supplemented with 0.20% fermented purslane. All data are presented as means ± SEM. *, p < 0.05.
Figure 3
Figure 3
Effects of dietary supplementation of FP on antioxidant indicators and intestinal permeability indicators of weaning piglets (n = 8). (A) Activity of SOD and CAT and concentration of T-AOC in serum; (B) concentration of MDA in serum; (C) activity of DAO and concentration of D-lactate in serum. SOD, superoxide dismutase; CAT, catalase; T-AOC, total antioxidant capacity; MDA, malondialdehyde; DAO, diamine oxidase; CON, piglets that were fed a standard corn–soybean meal basal diet; FP, piglets that were fed a basal diet supplemented with 0.20% fermented purslane. All data are presented as means ± SEM. *, p < 0.05.
Figure 4
Figure 4
Effects of dietary supplementation of FP on fecal microbiota in weaning piglets (n = 8). (A) α-Diversity; (B) PCoA plot depicting β-diversity of fecal microbiota based on Bray–Curtis distance. CON, piglets that were fed a standard corn–soybean meal basal diet; FP, piglets that were fed a basal diet supplemented with 0.20% fermented purslane. All data are presented as means ± SEM.
Figure 5
Figure 5
Effects of dietary supplementation of FP on fecal microbial composition in weaning piglets (n = 8). (A) Fecal microbiota composition shown at phylum level; (B) fecal microbiota composition shown at genus level; (C) LEfSe analysis of differential enrichment of fecal bacteria at genus level (linear discriminant analysis [LDA] > 3). CON, piglets that were fed a standard corn–soybean meal basal diet; FP, piglets that were fed a basal diet supplemented with 0.20% fermented purslane.
Figure 6
Figure 6
Effects of dietary supplementation of FP on fecal microbial enzymes based on the PICRUSt2 function prediction analysis in weaning piglets (n = 8). (A) The PCA plot is based on the enzymes; (B) the relative abundance of microbial enzymes related to SCFA synthesis. EC 1.1.1.27, L-lactate dehydrogenase; EC 2.3.1.8, phosphate acetyltransferase; EC 2.7.2.1, acetate kinase; EC 1.2.7.4, carbon-monoxide dehydrogenase (ferredoxin); EC 6.4.1.3, propionyl-CoA carboxylase; EC 5.4.99.22, methyl-malonyl-CoA mutase; EC 2.8.3.9, butyryl-CoA: acetate CoA-transferase; EC 2.7.2.7, butyrate kinase; EC 2.3.1.19, phosphate butyryl-transferase; CON, piglets that were fed a standard corn–soybean meal basal diet; FP, piglets that were fed a basal diet supplemented with 0.20% fermented purslane. All data are presented as means ± SD. *, p < 0.05; **, p < 0.01.
Figure 7
Figure 7
Effects of dietary supplementation of FP on concentration of SCFAs in feces of weaning piglets (n = 8). SCFAs, short-chain fatty acids; CON, piglets that were fed a standard corn–soybean meal basal diet; FP, piglets that were fed a basal diet supplemented with 0.20% fermented purslane. All data are presented as means ± SEM. *, p < 0.05.
Figure 8
Figure 8
The Spearman correlations among the relative abundance of significantly altered fecal microbiota, microbiota encoding enzymes related to butyrate synthesis, and the concentration of SCFAs. EC 2.8.3.9, butyryl-CoA: acetate CoA-transferase; EC 2.7.2.7, butyrate kinase; EC 2.3.1.19, phosphate butyryl-transferase; SCFAs, short-chain fatty acids. *, p < 0.05; **, p < 0.01; ***, p < 0.001.
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