Response of Salmonella enterica serovar Typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses

Jiaying Cheng , Mengshi Xiao , Xinmiao Ren , Francesco Secundo , Ying Yu , Shihao Nan , Weimiao Chen , Changliang Zhu , Qing Kong , Youtao Huang , Xiaodan Fu , Haijin Mou

Marine Life Science & Technology ›› 2023, Vol. 5 ›› Issue (2) : 242 -256.

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Marine Life Science & Technology ›› 2023, Vol. 5 ›› Issue (2) : 242 -256. DOI: 10.1007/s42995-023-00176-z
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Response of Salmonella enterica serovar Typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses

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Abstract

Alginate oligosaccharides (AOS), extracted from marine brown algae, are a common functional feed additive; however, it remains unclear whether they modulate the gut microbiota and microbial metabolites. The response of Salmonella enterica serovar Typhimurium, a common poultry pathogen, to AOS fermented with chicken fecal inocula was investigated using metabolomic and transcriptomic analyses. Single-strain cultivation tests showed that AOS did not directly inhibit the growth of S. Typhimurium. However, when AOS were fermented by chicken fecal microbiota, the supernatant of fermented AOS (F-AOS) exhibited remarkable antibacterial activity against S. Typhimurium, decreasing the abundance ratio of S. Typhimurium in the fecal microbiota from 18.94 to 2.94%. Transcriptomic analyses showed that the 855 differentially expressed genes induced by F-AOS were mainly enriched in porphyrin and chlorophyll metabolism, oxidative phosphorylation, and Salmonella infection-related pathways. RT-qPCR confirmed that F-AOS downregulated key genes involved in flagellar assembly and the type III secretory system of S. Typhimurium, indicating metabolites in F-AOS can influence the growth and metabolism of S. Typhimurium. Metabolomic analyses showed that 205 microbial metabolites were significantly altered in F-AOS. Among them, the increase in indolelactic acid and 3-indolepropionic acid levels were further confirmed using HPLC. This study provides a new perspective for the application of AOS as a feed additive against pathogenic intestinal bacteria.

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Jiaying Cheng, Mengshi Xiao, Xinmiao Ren, Francesco Secundo, Ying Yu, Shihao Nan, Weimiao Chen, Changliang Zhu, Qing Kong, Youtao Huang, Xiaodan Fu, Haijin Mou. Response of Salmonella enterica serovar Typhimurium to alginate oligosaccharides fermented with fecal inoculum: integrated transcriptomic and metabolomic analyses. Marine Life Science & Technology, 2023, 5(2): 242-256 DOI:10.1007/s42995-023-00176-z

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