Interaction between bacterial microbiota and nematode parasite communities in sheep's gastrointestinal tract

Abstract

The economic impact of gastrointestinal (GI) nematode infections on livestock production is well documented worldwide. Increasing evidence supports the hypothesis that parasite colonization induces significant changes in the GI tract environment and, therefore, in the landscape where the microbiota and parasites occur. Understanding the interactions between bacterial and parasite populations in the digestive tract of livestock may be useful to design parasite control strategies based on microbiota modification. The aims of this work were to investigate the impact of the oxytetracycline-mediated manipulation of the gut microbial community on the composition of GI nematode populations in naturally infected sheep and to explore changes in the GI microbial communities after nematode population treatment with the anthelmintic compound monepantel. Extensive manipulation of the GI microbiota with a therapeutic dose of the long-acting oxytetracycline formulation did not induce significant changes in the GI nematode burden. The gut microbiota of treated animals returned to control levels 17 days after treatment, suggesting strong resilience of the sheep microbial community to antibiotic-mediated microbiota perturbation. A significant decrease of the bacterial Mycoplasmataceae family (Log2FC = -4, Padj = 0.001) and a marked increase of the Methanobacteriaceae family (Log2FC = 2.9, Padj = 0.018) were observed in the abomasum of sheep receiving the monepantel treatment. While a comprehensive evaluation of the interactions among GI mycoplasma, methanobacteria and nematode populations deserves further assessment, the bacteria-nematode population interactions should be included in future control programs in livestock production. Understanding how bacteria and parasites may influence each other in the GI tract environment may substantially contribute to the knowledge of the role of microbiota composition in nematode parasite establishment and the role of the parasites in the microbiota composition.

Fig 1. Nematode abundance in the gastrointestinal tract of untreated (Control) sheep and sheep treated with long acting oxytetracycline (OTC-LA).

The relative proportion of each parasite species present in each animal belonging to Control (C1-C5) and OTC-LA (OTC1-OTC5) groups, as determined by nemabiome metabarcoding (ITS-2 rDNA deep-amplicon sequencing), is indicated.

Fig 2. Differential abundance of Mycoplasmatacea and Methanobacteriaceae families in the abomasum of Control and monepantel (MNP)-treated sheep.

The boxplot shows the normalized counts of Mycoplasmatacea and Methanobacteriaceae families in the abomasum of Control and monepantel (MNP) groups. The horizontal dashed lines represent the median values for each corresponding value. Dots are observations of each animal.

Fig 3. Estimates of microbiota richness in sheep from Control, monepantel (MNP) and long-acting oxytetracycline (OTC-LA) groups.

The boxplot shows the observed values of the Shannon Index for the abomasum (A) and the large intestine (B) across 15 animals from Control, MNP and OTC-LA groups. The horizontal dashed lines represent the median values for each corresponding microbiota. Dots are observations of each animal.

Fig 4. Principal coordinate plots representing beta diversity on samples.

The plots show comparison of microbiota diversity among monepantel (MNP), long acting oxytetracycline (OTC-LA) and Control groups. (A) Principal coordinate analysis (PCoA) of Bray-Curtis distances for abomasum. (B) PCoA of unweighted UniFrac distances for abomasum. (C) PCoA of Bray-Curtis distances for large intestine. (D) PCoA of unweighted UniFrac distances for large intestine. Sheep from each group are identified with colored dots.