Endotoxin lipopolysaccharide challenge triggers gut microbiota dysbiosis and host immune remodeling in the tiger grouper Epinephelus fuscoguttatus.

Abstract

Lipopolysaccharide (LPS) is a bacterial endotoxin that can trigger immune responses in aquatic animals. The gut microbiota is crucial for nutrient absorption and immune regulation in fish. In this study, the tiger grouper Epinephelus fuscoguttatus was selected as an animal model to investigate the effects of LPS challenge on the composition and function of gut microbiota and the gene transcriptional profiles of head kidney. The results showed that LPS challenge slightly increased gut microbial diversity indices (ACE, Simpson) and decreased Chao1 and Shannon indices; it also increased the abundances of Proteobacteria and harmful bacteria (Vibrio, Pseudomonas), while decreased those of Firmicutes, Actinobacteria and beneficial bacteria (Collinsella, Romboutsia) that produce short-chain fatty acids. The predicted carbohydrate and protein digestion/absorption functions of gut microbiota were significantly weakened. Additionally, LPS challenge induced 757 up- and 379 down-regulated genes in the head kidney, mainly involved in DNA replication, aminoacyl-tRNA biosynthesis and two-component system. Immune-related genes including pattern recognition receptors TLR1/2 was up-regulated but TLR3 was down-regulated; immune regulation (PIgR, MHC2), apoptosis (Cytc, Casp3, BIRC5), stress response (HSP60/70/90, GRP94, Bip, HURP1) and iron homeostasis (Mfn1, TFR1, Hepc) related genes were up-regulated; complement (C1QL3, C1QBP, C7), chemokines and their receptors (LECT2, CXCR3/1/4, CCR2) related genes showed disordered expression. Several bacterial genera groups, such as Collinsella, Romboutsia, Phyllobacterium, Prevotella 9, and Prevotellaceae NK3B31, were positively associated with the changes in host immune function. These findings demonstrated that LPS challenge induced the structural perturbations of gut microbiota, and disrupted the immune homeostasis of the head kidney of the grouper.