The development and excretion of Toxoplasma gondii oocyst manipulate the gut microbiota in its definitive host

TL;DR

This study shows how Toxoplasma gondii oocyst development affects the gut microbiome of cats, potentially offering new ways to control the spread of the parasite.

Contribution

The study identifies specific bacterial changes and pathways linked to oocyst excretion, highlighting Bacteroides stercoris as a key player.

Findings

Oocyst development alters gut microbiota function and diversity, with significant changes in KEGG pathways and CAZymes.

Bacteroides stercoris is significantly upregulated and may influence oocyst excretion through CBMs and GHs.

Probiotics and LA-related bacteria are dominant during oocyst development, suggesting potential for intervention strategies.

Abstract

Oocysts serve as the primary source of Toxoplasma infection. Therefore, understanding oocyst development and exploring effective strategies to prevent oocyst excretion are crucial for controlling toxoplasmosis.

In this study, shotgun metagenomics was employed to characterize the functional and compositional changes in the gut microbiota of cats during oocyst development. The Spearman correlation test was utilized to analyze the correlation between differential Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways and carbohydrate-active enzymes (CAZymes) in key bacteria regulating oocyst excretion.

The results revealed that group A (sexual initiation stage) displayed a lower number of functional genes, which were restored to normal levels in group B (oocyst excretion stage), compared with group C (Toxoplasma-uninfected samples). The abundance of 39 KEGG pathways, 106 CAZymes, and 98 virulence factors (VFs) varied significantly among the three groups. The atrazine degradation pathway, associated with sexual development, was upregulated in group B. CAZymes involved in restoring the intestinal mucosal barrier and VFs related to iron metabolism, antibiotic resistance, and suppression of host immunity were enriched in group B. Sexual initiation and oocyst excretion resulted in reduced gut bacterial diversity and microbiota dysbiosis. Probiotics and bacteria related to linoleic acid (LA) uptake were dominant in both group A and group B. Bacteroides stercoris was the most significantly upregulated bacterium and could influence the expression of carbohydrate-binding modules (CBMs) and glycoside hydrolases (GHs) in group B.

During the oocyst development/excretion stage, the function and composition of the cat gut microbiota changed significantly. In addition, Bacteroides stercoris may play a crucial role in oocyst excretion by regulating key candidates of CBMs and GHs. Our findings lay the foundation for investigating the regulatory mechanisms of oocyst excretion.

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