Dietary Supplementation With Lactobacillus plantarum Ameliorates Compromise of Growth Performance by Modulating Short-Chain Fatty Acids and Intestinal Dysbiosis in Broilers Under Clostridium perfringens Challenge.

Baikui Wang,Xiang Li,Yuanhao Zhou,Qianpeng Guo,Li Gong,Weifen Li,Huihua Zhang,Yulong Mao,Fei Wang,Shujie Xu

doi:10.3389/fnut.2021.706148

Abstract

Clostridium perfringens is an important zoonotic pathogen associated with food contamination and poisoning, gas gangrene, necrotizing enterocolitis or necrotic enteritis in humans and animals. Dysbacteriosis is supposedly associated with the development of C. perfringens infection induced necrotic enteritis, but the detailed relationship between intestinal health, microbiome, and C. perfringens infection-induced necrotic enteritis remains poorly understood. This research investigated the effect of probiotics on the growth performance and intestinal health of broilers, and the involved roles of intestinal microbiota and microbial metabolic functions under C. perfringens infection. Results showed that subclinical necrotic enteritis was successfully induced as evidenced by the significant lower body weight (BW), suppressed feed conversion ratio (FCR), decreased ileal villus height and mucosal barrier function, and increased ileal histopathological score and bursal weight index. Lactobacillus plantarum or Paenibacillus polymyxa significantly attenuated C. perfringens-induced compromise of growth performance (BW, FCR) and ileal mucosa damage as illustrated by the increased ileal villus height and villus/crypt ratio, the decreased ileal histopathological score and the enhanced ileal mucosal barrier function. L. plantarum also significantly alleviated C. perfringens-induced enlarged bursa of fabricius and the decreased levels of ileal total SCFAs, acetate, lactate, and butyrate. Furthermore, dietary L. plantarum improved C. perfringens infection-induced intestinal dysbiosis as evidenced by significantly enriched short-chain fatty acids-producing bacteria (Lachnospiraceae, Ruminococcaceae, Oscillospira, Faecalibacterium, Blautia), reduced drug-resistant bacteria (Bacteroides, Alistipes) and enteric pathogens (Escherichia coli, Bacteroides fragilis) and bacterial metabolic dysfunctions as illustrated by significantly increased bacterial fatty acid biosynthesis, decreased bacterial lipopolysaccharide biosynthesis, and antibiotic biosynthesis (streptomycin and vancomycin). Additionally, the BW and intestinal SCFAs were the principal factors affecting the bacterial communities and microbial metabolic functions. The above findings indicate that dietary with L. plantarum attenuates C. perfringens-induced compromise of growth performance and intestinal dysbiosis by increasing SCFAs and improving intestinal health in broilers.

Highlights

Clostridium perfringens (C. perfringens) is a widely distributed anaerobic spore-forming zoonotic pathogen, which causes foodborne illnesses in humans and necrotic enteritis in animals [1, 2]
Subclinical necrotic enteritis infection accompanies with continuously chronic damage of the gastrointestinal mucosa, which leads to poor growth performance of broilers with or without mortality [9, 35]
L. plantarum supplementation significantly reduced Bacteroidetes, drug-resistant bacteria (Bacteroides, Alistipes) [66, 67], and enteric pathogens (Escherichia coli, Bacteroides fragilis) [66], which may partly contribute to the inhibition of bacterial LPS biosynthesis and antibiotic biosynthesis. These findings indicated that L. plantarummediated-ameliorated compromise of growth performance in C. perfringens-infected broilers may be related to the restored gut microbial communities and bacterial metabolic functions, which should be further confirmed by whole shotgun metagenomic sequencing because of the limited taxonomical and functional attributes offered by 16S rRNA gene sequencing

Summary

Introduction

Clostridium perfringens (C. perfringens) is a widely distributed anaerobic spore-forming zoonotic pathogen, which causes foodborne illnesses in humans and necrotic enteritis in animals [1, 2]. Necrotic enteritis induced by C. perfringens is a widespread avian intestinal necrotic disease, which is estimated to cause the total global economic loss in poultry industry to be over US$6 billion annually [3]. Infeed antibiotics used to be the main strategy for preventing or controlling necrotic enteritis in poultry production. With the increasing public concerns about antimicrobial resistance and antibiotic residues in food animal products, infeed antimicrobial growth promoters have been widely removed from the animal feed by increasing global countries [6, 7]. The withdrawal of infeed prophylactic antibiotics and outbreaks of necrotic enteritis in the commercial poultry industry inspires an interest in seeking effective alternative antimicrobial strategies to prevent or control necrotic enteritis outbreaks. Multiple dietary alternatives to prophylactic antibiotics, such as probiotics, prebiotics, plant extracts, enzymes, and organic acids, have been proved to be effective in reducing or abolishing C. perfringensinduced necrotic enteritis [5, 9]

Results

Discussion

Conclusion