Integrated application of transcriptomics and metabolomics provides insight into the mechanism of Eimeria tenella resistance to maduramycin
Avian coccidiosis, caused by Eimeria parasites, continues to devastate the poultry industry and results in significant economic losses. Ionophore coccidiostats, such as maduramycin and monensin, are widely used for prophylaxis of coccidiosis in poultry. Nevertheless, their efficacy has been challeng...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-04-01
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| Series: | International Journal for Parasitology: Drugs and Drug Resistance |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211320724000071 |
| _version_ | 1797300385471266816 |
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| author | Huanzhi Zhao Hui Dong Qiping Zhao Shunhai Zhu Liushu Jia Sishi Zhang Qian Feng Yu Yu Jinwen Wang Bing Huang Hongyu Han |
| author_facet | Huanzhi Zhao Hui Dong Qiping Zhao Shunhai Zhu Liushu Jia Sishi Zhang Qian Feng Yu Yu Jinwen Wang Bing Huang Hongyu Han |
| author_sort | Huanzhi Zhao |
| collection | DOAJ |
| description | Avian coccidiosis, caused by Eimeria parasites, continues to devastate the poultry industry and results in significant economic losses. Ionophore coccidiostats, such as maduramycin and monensin, are widely used for prophylaxis of coccidiosis in poultry. Nevertheless, their efficacy has been challenged by widespread drug resistance. However, the underlying mechanisms have not been revealed. Understanding the targets and resistance mechanisms to anticoccidials is critical to combat this major parasitic disease. In the present study, maduramycin-resistant (MRR) and drug-sensitive (DS) sporozoites of Eimeria tenella were purified for transcriptomic and metabolomic analysis. The transcriptome analysis revealed 5016 differentially expressed genes (DEGs) in MRR compared to DS, and KEGG pathway enrichment analysis indicated that DEGs were involved in spliceosome, carbon metabolism, glycolysis, and biosynthesis of amino acids. In the untargeted metabolomics assay, 297 differentially expressed metabolites (DEMs) were identified in MRR compared to DS, and KEGG pathway enrichment analysis indicated that these DEMs were involved in 10 pathways, including fructose and mannose metabolism, cysteine and methionine metabolism, arginine and proline metabolism, and glutathione metabolism. Targeted metabolomic analysis revealed 14 DEMs in MRR compared to DS, and KEGG pathway analysis indicated that these DEMs were involved in 20 pathways, including fructose and mannose metabolism, glycolysis/gluconeogenesis, and carbon metabolism. Compared to DS, energy homeostasis and amino acid metabolism were differentially regulated in MRR. Our results provide gene and metabolite expression landscapes of E. tenella following maduramycin induction. This study is the first work involving integrated transcriptomic and metabolomic analyses to identify the key pathways to understand the molecular and metabolic mechanisms underlying drug resistance to polyether ionophores in coccidia. |
| first_indexed | 2024-03-07T23:06:26Z |
| format | Article |
| id | doaj.art-c1456fd963b64f80b80f3122fd606cc9 |
| institution | Directory Open Access Journal |
| issn | 2211-3207 |
| language | English |
| last_indexed | 2024-03-07T23:06:26Z |
| publishDate | 2024-04-01 |
| publisher | Elsevier |
| record_format | Article |
| series | International Journal for Parasitology: Drugs and Drug Resistance |
| spelling | doaj.art-c1456fd963b64f80b80f3122fd606cc92024-02-22T04:52:07ZengElsevierInternational Journal for Parasitology: Drugs and Drug Resistance2211-32072024-04-0124100526Integrated application of transcriptomics and metabolomics provides insight into the mechanism of Eimeria tenella resistance to maduramycinHuanzhi Zhao0Hui Dong1Qiping Zhao2Shunhai Zhu3Liushu Jia4Sishi Zhang5Qian Feng6Yu Yu7Jinwen Wang8Bing Huang9Hongyu Han10Key Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, CAAS, Shanghai, 200241, ChinaKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, CAAS, Shanghai, 200241, ChinaKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, CAAS, Shanghai, 200241, ChinaKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, CAAS, Shanghai, 200241, ChinaKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, CAAS, Shanghai, 200241, ChinaKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, CAAS, Shanghai, 200241, ChinaKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, CAAS, Shanghai, 200241, ChinaKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, CAAS, Shanghai, 200241, ChinaKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, CAAS, Shanghai, 200241, ChinaKey Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, CAAS, Shanghai, 200241, ChinaCorresponding author.; Key Laboratory of Animal Parasitology of Ministry of Agriculture, Shanghai Veterinary Research Institute, CAAS, Shanghai, 200241, ChinaAvian coccidiosis, caused by Eimeria parasites, continues to devastate the poultry industry and results in significant economic losses. Ionophore coccidiostats, such as maduramycin and monensin, are widely used for prophylaxis of coccidiosis in poultry. Nevertheless, their efficacy has been challenged by widespread drug resistance. However, the underlying mechanisms have not been revealed. Understanding the targets and resistance mechanisms to anticoccidials is critical to combat this major parasitic disease. In the present study, maduramycin-resistant (MRR) and drug-sensitive (DS) sporozoites of Eimeria tenella were purified for transcriptomic and metabolomic analysis. The transcriptome analysis revealed 5016 differentially expressed genes (DEGs) in MRR compared to DS, and KEGG pathway enrichment analysis indicated that DEGs were involved in spliceosome, carbon metabolism, glycolysis, and biosynthesis of amino acids. In the untargeted metabolomics assay, 297 differentially expressed metabolites (DEMs) were identified in MRR compared to DS, and KEGG pathway enrichment analysis indicated that these DEMs were involved in 10 pathways, including fructose and mannose metabolism, cysteine and methionine metabolism, arginine and proline metabolism, and glutathione metabolism. Targeted metabolomic analysis revealed 14 DEMs in MRR compared to DS, and KEGG pathway analysis indicated that these DEMs were involved in 20 pathways, including fructose and mannose metabolism, glycolysis/gluconeogenesis, and carbon metabolism. Compared to DS, energy homeostasis and amino acid metabolism were differentially regulated in MRR. Our results provide gene and metabolite expression landscapes of E. tenella following maduramycin induction. This study is the first work involving integrated transcriptomic and metabolomic analyses to identify the key pathways to understand the molecular and metabolic mechanisms underlying drug resistance to polyether ionophores in coccidia.http://www.sciencedirect.com/science/article/pii/S2211320724000071TranscriptomicMetabolomicsEimeria tenellaDrug resistanceMaduramycin |
| spellingShingle | Huanzhi Zhao Hui Dong Qiping Zhao Shunhai Zhu Liushu Jia Sishi Zhang Qian Feng Yu Yu Jinwen Wang Bing Huang Hongyu Han Integrated application of transcriptomics and metabolomics provides insight into the mechanism of Eimeria tenella resistance to maduramycin International Journal for Parasitology: Drugs and Drug Resistance Transcriptomic Metabolomics Eimeria tenella Drug resistance Maduramycin |
| title | Integrated application of transcriptomics and metabolomics provides insight into the mechanism of Eimeria tenella resistance to maduramycin |
| title_full | Integrated application of transcriptomics and metabolomics provides insight into the mechanism of Eimeria tenella resistance to maduramycin |
| title_fullStr | Integrated application of transcriptomics and metabolomics provides insight into the mechanism of Eimeria tenella resistance to maduramycin |
| title_full_unstemmed | Integrated application of transcriptomics and metabolomics provides insight into the mechanism of Eimeria tenella resistance to maduramycin |
| title_short | Integrated application of transcriptomics and metabolomics provides insight into the mechanism of Eimeria tenella resistance to maduramycin |
| title_sort | integrated application of transcriptomics and metabolomics provides insight into the mechanism of eimeria tenella resistance to maduramycin |
| topic | Transcriptomic Metabolomics Eimeria tenella Drug resistance Maduramycin |
| url | http://www.sciencedirect.com/science/article/pii/S2211320724000071 |
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