Fish-derived Probiotic Improves Growth Performance and Pathogen Resistance of Juvenile Grass Carp (Ctenopharyngodon idella) by Modulating Keystone Taxa and Enhancing Microbial Interactions

Abstract

Abstract Host-derived probiotics are bacteria isolated from the host's gut to improve the host’s growth and health. With more stringent antibiotic prohibitions in animal production, in-feed probiotics are becoming an appealing alternative to antibiotics in aquaculture. To explore the effects of Pseudomonas monteilii JK-1 on grass carp growth performance and disease resistance, 180 apparently healthy juvenile grass carp (3 ± 0.05 g) were randomly separated into 2 groups, each of which had 3 duplicates and 30 grass carp per replicate. Fish were fed with basal diets (control) or basal diets supplemented with P. monteilii JK-1 (1 × 107 CFU/g diet, PM-JK1) for 8 weeks. Results showed that P. monteilii JK-1 significantly increased the weight gain (WG), specific growth rate (SGR), survival rate and significantly reduced the pathogen load in grass carp (P < 0.05). Moreover, P. monteilii JK-1 supplementation significantly improved the expression of interleukin 1β (IL-1β), interleukin 10 (IL10), tumor necrosis factor alpha (TNF-α), and transforming growth factor beta (TGF-β) in head kidney and gut (P < 0.05). Furthermore, dietary supplementation with P. monteilii JK-1 significantly enhanced the activities of superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPx) in liver and gut (P < 0.05). The results of high-throughput sequencing revealed that P. monteilii JK-1 showed no significant influence on the composition of gut bacteria, but prevented changes of microbial community caused by A. hydrophila infection. Additionally, a network-based approach was used to analyze the influence of P. monteilii JK-1 on the interspecies relationships among the gut microbiome. The results showed that P. monteilii JK-1 supplementation improved the complexity of the gut ecological network. Further analysis found that Cetobacterium was the keystone microbiota in maintaining interspecies interactions and the stability of the gut network. Finally, we used a partial least squares path model to prove that P. monteilii JK-1 did not directly improve growth performance and pathogen resistance but rather by regulating keystone taxa and gut network stability. These results suggest that P. monteilii JK-1 could be used as a feed supplement to improve the growth performance and pathogen resistance of grass carp.