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. 2023 Sep 28:10:1253778.
doi: 10.3389/fvets.2023.1253778. eCollection 2023.

Metagenomic characterization of the cecal microbiota community and functions in finishing pigs fed fermented Boehmeria nivea

Xiaoxiao Liang  1 , Zhenya Zhai  2   3 , Fengyun Ren  4 , Yucheng Jie  4 , Soo-Ki Kim  5 , Kai-Min Niu  2   3 , Xin Wu  2   3   6
Affiliations

Metagenomic characterization of the cecal microbiota community and functions in finishing pigs fed fermented Boehmeria nivea

Xiaoxiao Liang et al. Front Vet Sci. .

Abstract

Ramie (Boehmeria nivea, BN) is used as livestock forage through suitable silage fermentation owing to its nutritional value. To date, relatively few studies have investigated the effects of dietary fermented BN (FBN) on gut health in finishing pigs. The aim of the present study was to investigate the effects of dietary supplementation with 20% FBN on intestinal morphology, gene expression, and the functional response of the gut microbiota in finishing pigs. We found that FBN did not significantly affect serum antioxidant enzyme activities, ileal morphology, or the expression of genes encoding antioxidant enzymes, inflammatory cytokines, or tight junction proteins in the liver of the pigs. However, the gene expression levels of aryl hydrocarbon receptor (AHR) and interleukin 6 (IL6) were significantly downregulated in the ileum. A metagenomic analysis demonstrated that, compared with that seen in the control group, the cecal microbiota of pigs in the FBN treatment group was more closely clustered and contained a greater number of unique microbes. Bacteria were the predominant kingdom in the cecal microbiota, while Firmicutes, Bacteroidetes, and Proteobacteria were the dominant phyla, and Streptococcus, Lactobacillus, and Prevotella were the dominant genera. Dietary FBN significantly increased the abundance of the probiotic bacterium Roseburia inulinivorans (p < 0.05). Functional analysis of the cecal microbiota showed that ABC transporter levels and glycolysis/gluconeogenesis-associated functions were diminished in FBN-fed pigs. Meanwhile, CAZyme analysis revealed that dietary FBN significantly downregulated the contents of carbohydrate-active enzymes, such as GT2, GH1, GH25, and GH13_31. In addition, cytochrome P450 analysis revealed that the abundance of CYP51 and CYP512 decreased with FBN treatment. An assessment of antibiotic resistance based on the Comprehensive Antibiotic Resistance Database (CARD) annotation indicated that the cecal microbes from pigs in the FBN treatment group had increased resistance to lincosamide, streptogramin, and chloramphenicol and reduced resistance to amikacin, isepamicin, neomycin, lividomycin, gentamicin, paromomycin, ribostamycin, and butirosin. Finally, virulence factor-related analysis showed that putative hemolysin-associated functions were decreased, whereas fibronectin-binding protein, flagella, and alginate-associated functions were increased. Taken together, our data showed that FBN supplementation exerted only minor effects on intestinal morphology and microbial community composition, suggesting that it is potentially safe for use as a supplement in the diets of finishing pigs. However, more studies are needed to validate its functionality.

Keywords: Boehmeria nivea; cecal microbiota; fermentation; metagenomics; pigs.

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Conflict of interest statement

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

Figures

Figure 1
Figure 1
Dietary effect of fermented Boechmeria nivea on ileal morphology of finishing pigs.
Figure 2
Figure 2
Dietary effects of fermented Boechmeria nivea on relative gene expression in liver (A) and ileum (B) of finishing pigs.
Figure 3
Figure 3
Principal component analysis of the similarity of the cecal microbiota.
Figure 4
Figure 4
Venn diagram showing the unique and shared species in the cecal microbiota.
Figure 5
Figure 5
The dominant cecal microbiome at the domain (A), kingdom (B), phylum (C), and genus (D) levels. *indicates significant differences at the level P < 0.05.
Figure 6
Figure 6
Putative probiotic abundance in the cecal microbiota annotated by the probiotic database.
Figure 7
Figure 7
Correlation analysis between the differentially altered species and gene expression.
Figure 8
Figure 8
Putative functions of the cecal microbiome annotated by the Kyoto Encyclopedia of Genes and Genomes (KEGG) at level 3.
Figure 9
Figure 9
Putative carbohydrate-active enzyme (CAZyme) abundances of cecal microbes at the family level, annotated using the CAZy database. GT, glycosyltransferases; GH, glycoside hydrolases; CE, carbohydrate esterases.
Figure 10
Figure 10
Putative CYP450 family of cecal microbes annotated using the Cytochrome P450 Engineering database.
Figure 11
Figure 11
Putative antibiotic resistance of cecal microbes at the class level annotated using the CARD database (Comprehensive Antibiotic Resistance Database). AR, Antibiotic resistance; AT, Antibiotic Target; AS, Antibiotic Sensitive; ABS, Antibiotic Biosynthesis.
Figure 12
Figure 12
Putative virulence factors of cecal microbes annotated by the Virulence Factor Database (VFDB).
See this image and copyright information in PMC

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Grants and funding

This work was financially supported by the pilot demonstration project for the Overall Rationing System of the Jiangxi Academy of Sciences (Grant Nos. 2022YSBG22002 and 2022YJC2002), the cooperation project of the Chinese Academy of Sciences and local governments (Grant No. 2022-03JXZT-02), the Key Collaborative Research Program of the Alliance of International Science Organizations (Grant No. ANSO-CR-KP-2021-10), and the Central Government Guides Local Science and Technology Development Fund of China (Grant No. 20231zdf03076).

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