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

Mingmin Lu,Hyun S Lillehoj,Youngsub Lee,Baohong Yuan,Charles Li,Xianghe Yan,Zhifeng Sun,Calder Baldwin-Bott

doi:10.3390/pathogens10121607

Abstract

Clostridium perfringens is an important opportunistic pathogen that may result in toxin-mediated diseases involving food poisoning/tissue gangrene in humans and various enterotoxaemia in animal species. It is a main etiological agent for necrotic enteritis (NE), the most financially devastating bacterial disease in broiler chickens, especially if raised under antibiotic-free conditions. Importantly, NE is responsible for losses of six billion US dollars annually in the global poultry industry. To investigate the molecular mechanisms of C. perfringens-induced pathogenesis in the gut and its microbiome mRNA levels in C. perfringens-infected and non-infected hosts, we used RNA sequencing technology to perform transcriptional analysis of both host intestine and microbiome using our NE model. The growth rate was significantly impaired in chickens infected by C. perfringens. In total, 13,473 annotated chicken genes were differentially expressed between these two groups, with ninety-six genes showing statistical significance (|absolute fold changes| > 2.0, adjusted p value < 0.05). Genes involved in energy production, MHC Class I antigen, translation, ribosomal structures, and amino acid, nucleotide and carbohydrate metabolism from infected gut tissues were significantly down-regulated. The upregulated genes were mainly engaged in innate and adaptive immunity, cellular processes, genetic information processing, and organismal systems. Additionally, the transcriptional levels of four crucial foodborne pathogens were significantly elevated in a synergic relationship with pathogenic C. perfringens infection. This study presents the profiling data that would likely be a relevant reference for NE pathogenesis and may provide new insights into the mechanism of host-pathogen interaction in C. perfringens-induced NE infection in broiler chickens.

Highlights

Clostridium perfringens is a Gram-positive, spore-forming anaerobe bacterium inducing opportunistic infection in humans and livestock worldwide [1]
On the basis of toxinotyping classification, namely based on the production of enterotoxin (CPE), NetB, α, β, ε, and ι- toxin, C. perfringens isolates are categorized into seven types (A-G) [5]
With next-generation RNA-Seq sequencing technology, we identified a plethora of differentially expressed genes (DEGs) in the small intestinal mucosa in response to C. perfringens infection

Summary

Introduction

Clostridium perfringens is a Gram-positive, spore-forming anaerobe bacterium inducing opportunistic infection in humans and livestock worldwide [1]. The successful transmission and colonization of C. perfringens strains in the hosts are mainly attributable to their survival patterns including oxygen sensitivity, sporulation, germination, and rapid proliferation capacity [3]. An arsenal of toxins (>20 identified toxins) produced by C. perfringens accounts for its virulence and pathogenesis in the host intestine or other organs [4]. In the United States, C. perfringens is one of the primary causes of non-foodborne diarrheal and foodborne diseases, with annual infected cases of approximately one million. The most common vehicle for C. perfringens infections is poultry and undercooked meat [6,7]

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