The response of cecal microbiota to inflammatory state induced by Salmonella enterica serovar Enteritidis

Abstract

By combining the experiments of reciprocal crosses of chicken infected with Salmonella enterica serovar Enteritidis (S. Enteritidis), we focused on the common response of cecal microbiota to an inflammatory state in respect of transcriptome and microbiome. The inoculation of S. Enteritidis improved the microbial diversity and promoted the microbiota evolution in our infection model. Correlation analysis between bacteria and inflammation-related genes showed that some intestinal microorganisms were “inflammophile” and thrived in an inflamed environment. The global function of cecal microbiome was to maintain the homeostasis likely by the up-regulation of microbial metabolism pathway in bacitracin, putrescine, and flavonoids production, although the bacitracin may affect the symbiotic bacteria Enterococcus. The action of S. Enteritidis had close relationships with multiple inflammation-related genes, including the genes PTAFR, LY96, and ACOD1 which proteins are related to the binding and tolerance of LPS, and the genes IL-18, IL-18R1 and IL-18RAP which products can form a functional complex and transmit IL-18 pro-inflammatory signal. Additionally, the infection of S. Enteritidis aroused the transcription of EXFABP, which protein has a potential to sequestrate the siderophore and might cause the decline of Escherichia-Shigella and Enterococcus. S. Enteritidis can escape from the sequestrating through the salmochelin, another kind of siderophore which cannot be recognized by EXFABP. Probably by this way, S. Enteritidis competed with the symbiotic bacteria and edged out the niches. Our research can help to understand the interplay between host, pathogen, and symbiotic bacteria.

Symbiotic bacteria stabilize the intestinal environment by producing phenylpropanoids

“…As described in our previous study (Hu, Liu, Miao, Zhao, Peng, et al, 2022), the result of 16S rRNA gene | 91 sequencing showed that S. Enteritidis was detected in a mean abundance of 1.09% (from 0.01% to 4.27%) in Salmonella groups (CT and RT) but not in control groups (CC and RC), suggesting S. Enteritidis can colonize in the cecal contents of chickens. We did not measure the colony-forming units of other organs.…”

“…It was reported that chicken genotype has a limited effect on resistance to S. Enteritidis infection between two inbred lines (Mon et al, 2015). Compared to the two regional chickens, their reciprocal crosses will be less influenced by genetic background and help us to find out the common response across hybrids, which had been reflected in our new studies (Hu, Liu, Miao, Zhao, & Li, 2022;Hu, Liu, Miao, Zhao, Peng, et al, 2022).…”

“…The details were described in our previous study (Hu, Liu, Miao, Zhao, Peng, et al, 2022 ). In brief, bacterial DNA was extracted from the samples of cecal contents using Soil DNA Kit (Omega, D5625‐01) according to manufacturer's protocols.…”

“…Although the studies on colonization resistance are plentiful in respect of the competition for conditions (oxygen, nutrition and niches) and the bacterial antibiotics (e.g. bacitracin), due to the complexity of intestinal microbiota, our understanding of this ecosystem remains incompletely characterized especially in the context of infection (Eckburg et al, 2005 ; Hooper & Gordon, 2001 ; Hu, Liu, Miao, Zhao, Peng, et al, 2022 ). Anchored in the basic biology of Salmonella infection, new technologies combined with careful experimental design will accelerate the discovery pipeline to define the mechanisms of immunity (Barrow et al, 2012 ).…”

Gene Co-Expression Network Analysis Reveals the Hub Genes and Key Pathways Associated with Resistance to Salmonella Enteritidis Colonization in Chicken

“…In this study, we also detected that the extracellular fatty acid binding protein (EXFABP) was significantly downregulated at 21 dpi compared to 7 dpi in chickens with low H/L ratio. In their study, Hu et al demonstrated that Salmonella Enteritidis (OTU607) was positively correlated with EXFABP among others genes, indicating that Salmonella Enteritidis infection arouses EXFABP transcription in chicken, which induces the sequestration of siderophore secreted by enteric bacteria and Gram-positive bacilli, such as Escherichia-Shigella and Enterococcus, resulting in a decrease of their abundance [50]. During infection, Salmonella escapes the antibacterial effect of EXFABP-mediated growth inhibition through salmochelin, which is not recognized by EXFABP [50].…”