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. 2024 Feb 14:15:1275865.
doi: 10.3389/fmicb.2024.1275865. eCollection 2024.

Ruminal microbiota and muscle metabolome characteristics of Tibetan plateau yaks fed different dietary protein levels

Kaiyue Pang #  1   2   3 , Jianmei Wang #  4 , Shatuo Chai  1   2   3 , Yingkui Yang  1   2   3 , Xun Wang  1   2   3 , Shujie Liu  1   2   3 , Cheng Ding  5 , ShuXiang Wang  1   2   3
Affiliations

Ruminal microbiota and muscle metabolome characteristics of Tibetan plateau yaks fed different dietary protein levels

Kaiyue Pang et al. Front Microbiol. .

Abstract

Introduction: The dietary protein level plays a crucial role in maintaining the equilibrium of rumen microbiota in yaks. To explore the association between dietary protein levels, rumen microbiota, and muscle metabolites, we examined the rumen microbiome and muscle metabolome characteristics in yaks subjected to varying dietary protein levels.

Methods: In this study, 36 yaks were randomly assigned to three groups (n = 12 per group): low dietary protein group (LP, 12% protein concentration), medium dietary protein group (MP, 14% protein concentration), and high dietary protein group (HP, 16% protein concentration).

Results: 16S rDNA sequencing revealed that the HP group exhibited the highest Chao1 and Observed_species indices, while the LP group demonstrated the lowest. Shannon and Simpson indices were significantly elevated in the MP group relative to the LP group (P < 0.05). At the genus level, the relative abundance of Christensenellaceae_R-7_group in the HP group was notably greater than that in the LP and MP groups (P < 0.05). Conversely, the relative abundance of Rikenellaceae_RC9_gut_group displayed an increasing tendency with escalating feed protein levels. Muscle metabolism analysis revealed that the content of the metabolite Uric acid was significantly higher in the LP group compared to the MP group (P < 0.05). The content of the metabolite L-(+)-Arabinose was significantly increased in the MP group compared to the HP group (P < 0.05), while the content of D-(-)-Glutamine and L-arginine was significantly reduced in the LP group (P < 0.05). The levels of metabolites 13-HPODE, Decanoylcarnitine, Lauric acid, L-(+)-Arabinose, and Uric acid were significantly elevated in the LP group relative to the HP group (P < 0.05). Furthermore, our observations disclosed correlations between rumen microbes and muscle metabolites. The relative abundance of NK4A214_group was negatively correlated with Orlistat concentration; the relative abundance of Christensenellaceae_R-7_group was positively correlated with D-(-)-Glutamine and L-arginine concentrations.

Discussion: Our findings offer a foundation for comprehending the rumen microbiome of yaks subjected to different dietary protein levels and the intimately associated metabolic pathways of the yak muscle metabolome. Elucidating the rumen microbiome and muscle metabolome of yaks may facilitate the determination of dietary protein levels.

Keywords: metabolomics; metabolomics yaks; microbiota; muscle; protein levels; rumen; yaks.

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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
Principal component analysis (PCA) of rumen bacterial community. Yaks with low (LP), medium (MP), and high (HP) dietary protein concentrations.
FIGURE 2
FIGURE 2
Rumen bacterial community composition. The dominant phylum (A) (top 10 relative abundance); genus (B) (top 10 relative abundance). Yaks with low (LP), medium (MP) and high (HP) dietary protein concentrations.
FIGURE 3
FIGURE 3
Significantly altered relative abundance of rumen bacteria of phylum (A,B) and genus (C,D). Different letters of ab in the graph indicate significantly different values (P < 0.05). Yaks with low (LP), medium (MP), and high (HP) dietary protein concentrations.
FIGURE 4
FIGURE 4
Orthogonal partial least squares discriminant analysis (OPLS-DA) scores for two-by-two comparison of metabolomics. Yaks with low (LP), medium (MP), and high (HP) dietary protein concentrations.
FIGURE 5
FIGURE 5
Heat map analysis of differential metabolite hierarchical clustering analysis for identifying VIP > 1 in muscle metabolism groups of yaks in LP, MP, and HP groups. Black squares represent the LP group, blue squares represent the MP group, and yellow squares represent the HP group. Each row represents one metabolite; each column represents one sample. The coloring is based on the signal intensity measured by LC-MS. Red represents high signal intensity, blue represents low signal intensity, and white cells represent intermediate (see the color scale on the right side of the heat map).
FIGURE 6
FIGURE 6
Volcano plot of differential metabolites for a two-by-two comparison (red represents up-regulated metabolites and green represents down-regulated metabolites). Yaks with low (LP), medium (MP), and high (HP) dietary protein concentrations.
FIGURE 7
FIGURE 7
Visual analysis of metabolic pathways by MetPA software with bubble plots. The size of the bubbles is proportional to the effect of each channel; bubble color represents significance, with red being the highest and white the lowest; P-values less than 0.05 and pathway impact factors greater than 0.5 indicate that the pathway is more affected.
FIGURE 8
FIGURE 8
Spearman’s correlation study between yak rumen bacterial genera and muscle differential metabolites. Each row in the figure represents a metabolite, each column represents a genus, and the color of each cell represents the Spearman correlation coefficient between metabolite and genus levels (red indicates positive correlation, blue indicates negative correlation). *P < 0.05, **P < 0.01.
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