Abstract
The gill and gastrointestinal tract are primary entry routes for pathogens. The symbiotic microbiota are essential to the health, nutrition and disease of fish. Though the intestinal microbiota of Nile tilapia (Oreochromis niloticus) has been extensively studied, information on the mucosa-associated microbiota of this species, especially the gill and gastrointestinal mucosa-associated microbiota, is lacking. This study aimed to characterize the gill and gastrointestinal mucosa- and digesta-associated microbiota, as well as the intestinal metabolite profiles in the New Genetically Improved Farmed Tilapia (NEW GIFT) strain of farmed adult Nile tilapia by high-throughput sequencing and gas chromatography/mass spectrometry metabolomics. The diversity, structure, composition, and predicted function of gastrointestinal microbiota were significantly different across gastrointestinal regions and sample types (Welch t-test; p < 0.05). By comparing the mucosa- and digesta-associated microbiota, linear discriminant analysis (LDA) effect size (LEfSe) analysis revealed that Pelomonas, Ralstonia pickettii, Comamonadaceae, and Staphylococcus were significantly enriched in the mucosa-associated microbiota, whereas many bacterial taxa were significantly enriched in the digesta-associated microbiota, including Chitinophagaceae, Cetobacterium, Candidatus Competibacter, Methyloparacoccus, and chloroplast (LDA score > 3.5). Furthermore, Undibacterium, Escherichia-Shigella, Paeniclostridium, and Cetobacterium were dominant in the intestinal contents and mucosae, whereas Sphingomonas aquatilis and Roseomonas gilardii were commonly found in the gill and stomach mucosae. The Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt2) analysis revealed that the predictive function of digesta-associated microbiota significantly differed from that of mucosa-associated microbiota (R = 0.8152, p = 0.0001). In addition, our results showed a significant interdependence between specific intestinal microbes and metabolites. Notably, the relative abundance values of several potentially beneficial microbes, including Undibacterium, Crenothrix, and Cetobacterium, were positively correlated with most intestinal metabolites, whereas the relative abundance values of some potential opportunistic pathogens, including Acinetobacter, Mycobacterium, Escherichia-Shigella, Paeniclostridium, Aeromonas, and Clostridium sensu stricto 1, were negatively correlated with most intestinal metabolites. This study revealed the characteristics of gill and gastrointestinal mucosa-associated and digesta-associated microbiota of farmed Nile tilapia and identified a close correlation between intestinal microbes and metabolites. The results serve as a basis for the effective application of targeted probiotics or prebiotics in the diet to regulate the nutrition and health of farmed tilapia.
Highlights
The microbiota of fish, like other vertebrates, play critical roles in host health and metabolism [1]
By comparing two types of digesta samples, we found that seven Operational taxonomic units (OTUs) belonging to Undibacterium, Paeniclostridium, SZB30, Candidatus Competibacter, and Rhizobiales Incertae Sedis were significantly enriched in the intestinal content samples, whereas 23 dominant OTUs were significantly enriched in the stomach content samples, including OTUs belonging to Chitinophagaceae, Verrucomicrobiae, Comamonadaceae, Novosphingobium, and chloroplast (Figure 5A)
By comparing the mucosa samples with the digesta samples, we found that five OTUs belonging to Pelomonas, R. pickettii, Comamonadaceae, and Staphylococcus were significantly enriched in the mucosa samples, whereas eleven OTUs were significantly enriched in the digesta samples, including OTUs belonging to Chitinophagaceae, Rhizobiales Incertae Sedis, chloroplast, HOC36, Cetobacterium, SZB30, Methyloparacoccus, and Candidatus Competibacter (Figure 5B)
Summary
The microbiota of fish, like other vertebrates, play critical roles in host health and metabolism [1]. Fish microbiota include resident communities (autochthonous or associated with mucosa) and transient communities (allochthonous or associated with digesta) [2]. Most infections start at or affect the fish mucosal epithelia. The mucosal surfaces of these organs represent an important barrier that supports and regulates a wide variety of microbial communities [2]. These diverse and balanced mucosa-associated microbial communities are essential for fish health [4], but the mechanism underlying their interactions with the host remains unclear
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