1H-NMR based-metabolomics reveals alterations in the metabolite profiles of chickens infected with ascarids and concurrent histomonosis infection

Oyekunle John Oladosu; Banny Silva Barbosa Correia; Beatrice Grafl; Dieter Liebhart; Cornelia C Metges; Hanne Christine Bertram; Gürbüz Daş

doi:10.1186/s13099-023-00584-7

¹H-NMR based-metabolomics reveals alterations in the metabolite profiles of chickens infected with ascarids and concurrent histomonosis infection

Gut Pathog. 2023 Nov 17;15(1):56. doi: 10.1186/s13099-023-00584-7.

Authors

Oyekunle John Oladosu¹, Banny Silva Barbosa Correia², Beatrice Grafl³, Dieter Liebhart³, Cornelia C Metges¹, Hanne Christine Bertram², Gürbüz Daş⁴

Affiliations

¹ Research Institute for Farm Animal Biology (FBN), Institute of Nutritional Physiology 'Oskar Kellner', Wilhelm-Stahl-Allee 2, 18196, Dummerstorf, Germany.
² Department of Food Science, Aarhus University, Agro Food Park 48, 8200, Aarhus N, Denmark.
³ Clinic for Poultry and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine, Vienna, Austria.
⁴ Research Institute for Farm Animal Biology (FBN), Institute of Nutritional Physiology 'Oskar Kellner', Wilhelm-Stahl-Allee 2, 18196, Dummerstorf, Germany. gdas@fbn-dummerstorf.de.

Abstract

Background: Gut infections of chickens caused by Ascaridia galli and Heterakis gallinarum are associated with impaired host performance, particularly in high-performing genotypes. Heterakis gallinarum is also a vector of Histomonas meleagridis that is often co-involved with ascarid infections. Here, we provide a first insight into the alteration of the chicken plasma and liver metabolome as a result of gastrointestinal nematode infections with concomitant histomonosis. ¹H nuclear magnetic resonance (¹H-NMR) based-metabolomics coupled with a bioinformatics analysis was applied to explore the variation in the metabolite profiles of the liver (N = 105) and plasma samples from chickens (N = 108) experimentally infected with A. galli and H. gallinarum (+H. meleagridis). This was compared with uninfected chickens at different weeks post-infection (wpi 2, 4, 6, 10, 14, 18) representing different developmental stages of the worms.

Results: A total of 31 and 54 metabolites were quantified in plasma and aqueous liver extracts, respectively. Statistical analysis showed no significant differences (P > 0.05) in any of the 54 identified liver metabolites between infected and uninfected hens. In contrast, 20 plasma metabolites including, amino acids, sugars, and organic acids showed significantly elevated concentrations in the infected hens (P < 0.05). Alterations of plasma metabolites occurred particularly in wpi 2, 6 and 10, covering the pre-patent period of worm infections. Plasma metabolites with the highest variation at these time points included glutamate, succinate, trimethylamine-N-oxide, myo-inositol, and acetate. Differential pathway analysis suggested that infection induced changes in (1) phenylalanine, tyrosine, and tryptophan metabolism, (2) alanine, aspartate and glutamate metabolism; and 3) arginine and proline metabolism (Pathway impact > 0.1 with FDR adjusted P-value < 0.05).

Conclusion: In conclusion, ¹H-NMR based-metabolomics revealed significant alterations in the plasma metabolome of high performing chickens infected with gut pathogens-A. galli and H. gallinarum. The alterations suggested upregulation of key metabolic pathways mainly during the patency of infections. This approach extends our understanding of host interactions with gastrointestinal nematodes at the metabolic level.

Keywords: Blackhead disease; Gastrointestinal infections; Helminths; Infection-induced metabolite alterations; Liver; Metabolome; Plasma; Poultry; Spectroscopy.

Abstract

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