Multi-Omics Analysis Reveals a Correlation between the Host Phylogeny, Gut Microbiota and Metabolite Profiles in Cyprinid Fishes

Abstract

Gut microbiota play key roles in host nutrition and metabolism. However, little is known about the relationship between host genetics, gut microbiota and metabolic profiles. Here, we used high-throughput sequencing and gas chromatography/mass spectrometry approaches to characterize the microbiota composition and the metabolite profiles in the gut of five cyprinid fish species with three different feeding habits raised under identical husbandry conditions. Our results showed that host species and feeding habits significantly affect not only gut microbiota composition but also metabolite profiles (ANOSIM, p ≤ 0.05). Mantel test demonstrated that host phylogeny, gut microbiota, and metabolite profiles were significantly related to each other (p ≤ 0.05). Additionally, the carps with the same feeding habits had more similarity in gut microbiota composition and metabolite profiles. Various metabolites were correlated positively with bacterial taxa involved in food degradation. Our results shed new light on the microbiome and metabolite profiles in the gut content of cyprinid fishes, and highlighted the correlations between host genotype, fish gut microbiome and putative functions, and gut metabolite profiles.

Keywords: correlation; cyprinid fishes; gut microbiota; host phylogeny; metabolite profiles.

FIGURE 1

Differences in the composition of gut microbial and metabolite profiles. Non-metric Multidimensional Scaling (NMDS) plot showing variation in the composition (Bray–Curtis distance) of gut bacterial communities (A) and metabolite profiles (B) among different fish species. Hierarchical clustering of sample groups based on the mean relative abundance of each OTU (C) and metabolite (D) in each fish species. Abbreviations: FS, silver carp; FB, bighead carp; HG, grass carp; HB, blunt snout bream; OC, crucian carp.

FIGURE 2

Bacterial composition of the different communities (relative read abundance of bacterial phyla within each community). Lanes FB1–FB3, FS1–FS3, HB1–HB3, HG1–HG3, and OC1–OC3 correspond to the three individuals of bighead carp, silver carp, blunt snout bream, grass carp, and crucian carp, respectively.

FIGURE 3

Summary of the variation in gut microbiota, gut metabolite, and evolutionary distance among different fish species. (A) A heat map of the mean abundances of the prominent OTUs (average abundance > 0.1%) assigned to genus level among different fish species. The rows represent the 63 predominant bacterial OTUs, and the values in the heatmap represent the Z-transformed relative percentage of each OTU. Phylum and genus level classifications of OTUs (OTU ID in parentheses) are noted also. (B) A heat map of the mean percent abundances of top50 metabolite among different fish species. Both heat map based on the same hierarchical clustering solution (Bray–Curtis distance metric and complete clustering method). (C) Phylogenetic tree of the five cyprinid fish species based on the concatenated sequences of the two mitochondrial genes. The numbers on the nodes are neighbor-joining bootstrap values (values > 50 are shown), and bootstrap was replicated 999 times. The bar shows the relative branch length distance computed using the Kimura 2-parameter method. HG, grass carp; HB, blunt snout bream; OC, crucian carp; FS, silver carp; and FB, bighead carp.

FIGURE 4

The correlation between some specific microbes and metabolite. (A) Top 24 OTUs that differentiate among different fish species as revealed by Random Forest. The phylum and genus classifications are also provided. The OTU ID is given after the genus. (B) Redundancy analysis (RDA) of some specific gut microbes responding to metabolite. Only those metabolite with relative abundances > 3% were shown.