Identification of an intestinal microbiota signature associated with the severity of necrotic enteritis

Authors: YANG, QING - Oklahoma State University; LIU, JING - Oklahoma State University; WANG, XIAOFAN - University Of Arkansas; Robinson, Kelsy; WHITMORE, MELANIE - Oklahoma State University; STEWART, SYDNEY - Oklahoma State University; ZHAO, JIANGCHAO - University Of Arkansas; ZHANG, GUOLONG - Oklahoma State University

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/27/2021
Publication Date: 8/19/2021
Citation: Yang, Q., Liu, J., Wang, X., Robinson, K., Whitmore, M.A., Stewart, S.N., Zhao, J., Zhang, G. 2021. Identification of an intestinal microbiota signature associated with the severity of necrotic enteritis. Frontiers in Microbiology. 12. Article 703693. https://doi.org/10.3389/fmicb.2021.703693.
DOI: https://doi.org/10.3389/fmicb.2021.703693

Interpretive Summary: Necrotic enteritis (NE) is an economically devastating disease of poultry that cause small intestinal lesions, growth retardation, reduced feed efficiency and high mortality. NE is associated with disruption of the intestinal bacterial population, known as the microbiota. However, the dynamics of this disruption and the species associated with disease severity are still unknown. Here, we investigated the link between the ileal microbiota and disease severity in a chicken model of clinical NE using 16S rRNA gene sequencing. Our results demonstrate a disease severity-dependent reduction in several bacterial species. In particular, a progressive decline in beneficial bacteria such as lactic acid and short chain fatty acid producing species was observed following NE infection. Additionally, functional analysis revealed a suppression of secondary bile acid biosynthesis in infected birds while biosynthesis of aromatic and branched-amino acids was enhanced. The outcomes of this study have provided a better understanding of disease pathogenesis and the microbiota-host interactions in the context of NE, which provides important leads for future development of novel microbiota-based diagnostic or therapeutic approaches for the control and prevention of NE in poultry.

Technical Abstract: Necrotic enteritis (NE), an economically devastating disease of poultry, is known to cause small intestinal lesions and dysbiosis. However, the microbes that are associated with NE severity is currently unknown. Here, we investigated the link between the ileal microbiota and disease severity in a chicken model of clinical NE using 16S rRNA gene sequencing. Our results indicated that richness and Shannon Index of the ileal microbiota were drastically reduced (P < 0.01) as NE was exacerbated. While Clostridium perfringens was increased from 0.02% or 2.6 × 102 CFU/g digesta in healthy chickens to 58-70% or 1.6-2.7 × 108 CFU/g digesta in chickens with severe infection, a majority of the ileal microbes were markedly diminished, albeit varying in their sensitivity to NE. Firmicutes such as Group A and B Lactobacillus, Lactobacillus reuteri, Subdoligranulum variabile, mediterraneibacter, and Staphylococcus as well as two genera of Actinobacteria (Corynebacterium and Kocuria) and two highly related Cyanobacteria were progressively declined as NE was aggravated. Other Firmicutes such as Weissella, Romboutsia, Kurthia, Cuneatibacter, Blautia, and Aerococcus appeared much more sensitive, becoming quickly abolished in chickens even with mild NE. On the other hand, Enterococcus cecorum and two Escherichia/Shigella species were only enriched in the ileal microbiota of chickens with extremely severe NE, while Streptococcus gallolyticus, Bacteroides fragilis, Fournierella massiliensis, Paeniclostridium sordellii, and a Proteus species remained unaltered by NE. Functionally, secondary bile acid biosynthesis was predicted to be suppressed by NE, while biosynthesis of aromatic and branched-amino acids was enhanced in the ileum of NE-afflicted chickens.