Clostridium perfringens-Induced Host-Pathogen Transcriptional Changes in the Small Intestine of Broiler Chickens

Authors: LU, MINGMIN - US Department Of Agriculture (USDA); YUAN, BAOHONG - US Department Of Agriculture (USDA); Yan, Xianghe; Sun, Zhifeng; Lillehoj, Hyun; LEE, YOUNGSUB - US Department Of Agriculture (USDA); Li, Charles

Submitted to: Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/4/2021
Publication Date: 12/10/2021
Citation: Lu, M., Yuan, B., Yan, X., Sun, Z., Lillehoj, H.S., Lee, Y., Li, C.Z. 2021. Clostridium perfringens-Induced Host-Pathogen Transcriptional Changes in the Small Intestine of Broiler Chickens. Pathogens. 10(12):1607. https://doi.org/10.3390/pathogens10121607.
DOI: https://doi.org/10.3390/pathogens10121607

Interpretive Summary: Clostridium perfringens (CP) is an important bacterium that is present ubiquitously in the environment and in the gastrointestinal tract of humans and animals. It can cause toxin-mediated diseases, including food poisoning /traumatic tissue necrosis in human and various intestinal complications in animal species. It is a main etiological agent for necrotic enteritis (NE) in boiler chickens which has conventionally been controlled by antibiotics, responsible for $6 billion losses annually in global poultry industry. During recent decades, increasing incidences of NE in poultry industry have been found to be associated with the voluntary reduction or withdrawal of antibiotic growth promoters from the food animal feed due to public concerns and governmental regulations. To effectively manage this economically important infectious disease, it is imperative to first understand the molecular mechanism of the effects of CP infection on the gene levels (called mRNA) of the intestines (as a host) and gut microbiological populations between the CP-infected and non-infected hosts. In this study, we used RNA sequencing technology to perform mRNA level analysis of both the intestinal host and the CP pathogen itself in chicken NE model. In total, 13473 annotated chicken genes showed differential expression between these two groups. Ninety-six significant genes were statistically differentially expressed (|absolute fold changes| >2.0). The intestinal tissues from CP-infected chickens had a significantly altered gene expression profile. In addition, some potential virulence factor genes were also identified in the CP bacteria in CP-infected chickens when compared with the uninfected control. It appeared that other food-borne pathogens were also active in a synergy with pathogenic CP infection. This study provides new insights into a range of factors involved in host-pathogen interaction following C. perfringens infection in broiler chickens.

Technical Abstract: Clostridium perfringens (CP) is an opportunistic pathogen that can cause food poisoning / tissue gangrene in human and various enterotoxaemia in animal species. It is a main etiological agent for necrotic enteritis (NE) in boiler chickens, responsible for $6 billion loss in global poultry industry. To investigate the molecular mechanism of the effects of CP infection on the host intestine and gut microbiome mRNA level between the Clostridium perfringens-infected and non-infected hosts, we used RNA sequencing technology to perform transcriptional analysis of both the intestinal host and the CP pathogen itself in chicken NE model. In total, 13473 annotated chicken genes showed differential expression between the two groups. Ninety-six significant genes were statistically differentially expressed between these two groups (|absolute fold changes| >2.0, adjust p value < 0.05). Genes that were down-regulated in infected cells, including those involved in energy production, amino acid, nucleotide and carbohydrate metabolism, and in translation and ribosomal structures. Genes up-regulated were mainly involved in adaptive immunity, cellular processes, environmental information processing, genetic information processing, diseases metabolism, and organismal systems. Some potential virulence genes were significantly upregulated in the CP bacteria in vivo in CP-infected chickens when compared with the uninfected control. It appeared that other food-borne pathogens were also active in a synergy with pathogenic CP infection. This study provides new insights into the mechanism of host-pathogen interaction following C. perfringens infection in broiler chickens.