Integration of metagenome and metabolome analysis reveals the correlation of gut microbiota, oxidative stress, and inflammation in Coilia nasus under air exposure stress and salinity mitigation

Abstract

Due to the strong response to air exposure, high mortality was occurred in Coilia nasus. Previous studies reported that 10 ‰ NaCl could significantly reduce mortality in C. nasus under air exposure. To investigate the mechanisms that 10 ‰ NaCl can alleviate stress, community structure and metabolism of the intestinal flora of C. nasus were detected via metagenome and metabolome. In this study, C. nasus were divided into control group (C), air exposure group without 10 ‰ NaCl (AE), and air exposure group with 10 ‰ NaCl (AES). After air exposure stress and salinity mitigation, the mortality, intestinal microorganisms, metabolites, and physiological biomarkers were analyzed. The results showed that the mortality rate of C. nasus was reduced after salinity reduction; the antioxidant capacity was elevated compared to the AE group; and anti-inflammatory capacity was increased in the AES group compared to the AE group. Metagenomic sequencing results showed that the levels of harmful bacteria (E. coli, Aeromonas) in the Candida nasus gut increased after air exposure; beneficial bacteria (Actinobacteria, Corynebacteria) in the C. nasus gut increased after salinity reduction. Metabolomics analyses showed that AE decreased the expression of beneficial metabolites and increased the expression of harmful metabolites; AES increased beneficial metabolites and decreased harmful metabolites. Correlation analysis showed that in the AE group, beneficial metabolites were negatively correlated with oxidative stress and inflammatory response, while harmful metabolites were positively correlated with oxidative stress and inflammatory response, and were associated with bacterial communities such as Gillisia, Alkalitalia, Avipoxvirus, etc.; the correlation of metabolites with oxidative stress and inflammatory response was opposite to that of AE in the case of AES, and was associated with Lentilactobacillus, Cyanobacterium, and other bacterial communities. Air exposure caused damage to Candida rhinoceros and 10 ‰ salinity was beneficial in alleviating C. nasus stress. These results will provide new insights into methods and mechanisms to mitigate stress in fish.