Phosphoproteomic Comparison of Four Eimeria tenella Life Cycle Stages.

Xueting Ma,Zhenxing Gong,Baohong Liu,Jianping Cai,Zigang Qu

doi:10.3390/ijms222212110

Abstract

Protein phosphorylation is an important post-translational modification (PTM) involved in diverse cellular functions. It is the most prevalent PTM in both Toxoplasma gondii and Plasmodium falciparum, but its status in Eimeria tenella has not been reported. Herein, we performed a comprehensive, quantitative phosphoproteomic profile analysis of four stages of the E. tenella life cycle: unsporulated oocysts (USO), partially sporulated (7 h) oocysts (SO7h), sporulated oocysts (SO), and sporozoites (S). A total of 15,247 phosphorylation sites on 9514 phosphopeptides corresponding to 2897 phosphoproteins were identified across the four stages. In addition, 456, 479, and 198 differentially expressed phosphoproteins (DEPPs) were identified in the comparisons SO7h vs. USO, SO vs. SO7h, and S vs. SO, respectively. Gene Ontology (GO) term and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses of DEPPs suggested that they were involved in diverse functions. For SO7h vs. USO, DEPPs were mainly involved in cell division, actin cytoskeleton organization, positive regulation of transport, and pyruvate metabolism. For SO vs. SO7h, they were related to the peptide metabolic process, translation, and RNA transport. DEPPs in the S vs. SO comparison were associated with the tricarboxylic acid metabolic process, positive regulation of ATPase activity, and calcium ion binding. Time course sequencing data analysis (TCseq) identified six clusters with similar expression change characteristics related to carbohydrate metabolism, cytoskeleton organization, and calcium ion transport, demonstrating different regulatory profiles across the life cycle of E. tenella. The results revealed significant changes in the abundance of phosphoproteins during E. tenella development. The findings shed light on the key roles of protein phosphorylation and dephosphorylation in the E. tenella life cycle.

Highlights

Coccidiosis is a damaging parasitic disease in chickens that inflicts huge economic losses on the poultry industry
15,247 phosphorylation sites on 9514 phosphopeptides corresponding to 2897 phosphoproteins were identified across the four stages of the E. tenella life cycle
Wang et al found that citrate synthase (EtCS), an important tricarboxylic acid (TCA) cycle enzyme in E. tenella, was highly expressed at the unsporulated oocyst stage, suggesting that it may provide energy for parasite development [21]

Summary

Introduction

Coccidiosis is a damaging parasitic disease in chickens that inflicts huge economic losses on the poultry industry. The intracellular protozoan parasite that causes cecal coccidiosis in chickens, belongs to the phylum Apicomplexa. It has a complex developmental life cycle with separate exogenous (sporogony) and endogenous (schizogony and gametogony) phases [1]. In the exogenous phase, unsporulated oocysts (non-infective) are shed in chicken feces and undergo sporogony (sporulation) under appropriate conditions to become infective. After oral ingestion of sporulated oocysts (SO), sporozoites are excysted, and they infect chicken intestinal epithelia, after which E. tenella enters an endogenous phase involving schizogony and gametogony. After fertilization (gametogony), unsporulated oocysts are expelled into the environment with feces, and they enter the exogenous phase [2,3]

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