Taxonomic and Functional Characteristics of the Gill and Gastrointestinal Microbiota and Its Correlation with Intestinal Metabolites in NEW GIFT Strain of Farmed Adult Nile Tilapia (Oreochromis niloticus)

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, Ralstoniapickettii, 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, CandidatusCompetibacter, Methyloparacoccus, and chloroplast (LDA score > 3.5). Furthermore, Undibacterium, Escherichia–Shigella, Paeniclostridium, and Cetobacterium were dominant in the intestinal contents and mucosae, whereas Sphingomonasaquatilis and Roseomonasgilardii 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 Clostridiumsensustricto 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.

Characterization of External Mucosal Microbiomes of Nile Tilapia and Grey Mullet Co-cultured in Semi-Intensive Pond Systems

“…The pond water had the lowest abundance of Proteobacteria , whereas it was highly enriched in the mullet gill. The dominance of Proteobacteria in the external microbiome of teleost fish has been indicated in previous studies ( Chiarello et al, 2015 ; Legrand et al, 2018 ; Zhang et al, 2019 ; Wu et al, 2021 ). Communities with enriched Proteobacteria may reflect the advantage of unique niche colonization for enhancing microbial growth ( Zhang et al, 2019 ) and a significant role in the microbiome mucosal barrier for this bacterial phyla.…”

“…Communities with enriched Proteobacteria may reflect the advantage of unique niche colonization for enhancing microbial growth ( Zhang et al, 2019 ) and a significant role in the microbiome mucosal barrier for this bacterial phyla. Interestingly, several opportunistic aquatic pathogens, such as Aeromonas , Vibrio , and Plesiomonas , belong to Proteobacteria ; and their presence may stimulate and maintain mucosal immunity ( Wu et al, 2021 ). The higher abundance of Proteobacteria in external microbial communities was followed by Fusobacteriota and Firmicutes , which have been reported as ubiquitous phyla in the external microbiome of the fish ( Reverter et al, 2017 ; Zhang et al, 2019 ; Wu et al, 2021 ).…”

“…Interestingly, several opportunistic aquatic pathogens, such as Aeromonas , Vibrio , and Plesiomonas , belong to Proteobacteria ; and their presence may stimulate and maintain mucosal immunity ( Wu et al, 2021 ). The higher abundance of Proteobacteria in external microbial communities was followed by Fusobacteriota and Firmicutes , which have been reported as ubiquitous phyla in the external microbiome of the fish ( Reverter et al, 2017 ; Zhang et al, 2019 ; Wu et al, 2021 ). Fusobacteriota was remarkably enriched in tilapia gill, whereas Firmicutes was enriched in the skin for both species.…”

Effects of dietary compound acidifiers supplementation on growth performance and intestinal health of juvenile American eels (Anguilla rostrata) cultured in cement tanks

“…Some species in Mycobacterium have been reported to enhance the immunity in aquatic species like salmonids without any negative effects (Prathiviraj et al, 2021). However, several studies indicated that Mycobacterium might be a potential opportunistic pathogen to cause chronic long-term persistent infections in the gut of zebra fish (Wang et al, 2021;Wu et al, 2021). In our study, the relative The Israeli Journal of Aquaculture -Bamidgeh • IJA.73.2021.1520998 abundance of Mycobacterium was higher in CAs group, while no intestine health problem was observed during the cultivation process.…”

Spoilage Investigation of Chill Stored Meagre (Argyrosomus regius) Using Modern Microbiological and Analytical Techniques

“…Indeed, seafood has been characterized as an ideal reservoir of pathogenic microbes that are closely related to human diseases (e.g., via the production of neurotoxin), such as some species belonging to the genus Clostridium e.g., C. botulinum , C. perfringens [ 40 , 41 ], the presence of which, is mainly linked with a potential sewage contamination [ 42 ]. Furthermore, Ralstonia was found to dominate in the gut of cultured sea bass, Nile Tilapia and Maryland blue crab [ 43 , 44 , 45 ]. This bacterial group may be responsible for an initial deterioration of sensory attributes, via the production of specific enzymes, closely linked to food/seafood spoilage, such as lipase [ 46 ].…”