Nematodes exposed to furfural acetone exhibit a species-specific vacuolar H+-ATPase response
Furfural acetone (FAc) is widely used as an additive by the food industry, as well as an intermediate in several fine chemical industries. Its nematicidal activity against the free-living model organism Caenorhabditis elegans and the parasitic nematode Meloidogyne incognita are well known, but its m...
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| Format: | Article |
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Elsevier
2024-12-01
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| Series: | Ecotoxicology and Environmental Safety |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0147651324014830 |
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| author | Wanli Cheng Wei Dai Wen Chen Hua Xue Zhengzheng Zhao Zhengbing Jiang Huanan Li Jiashu Liu Feng Huang Minmin Cai Longyu Zheng Ziniu Yu Donghai Peng Jibin Zhang |
| author_facet | Wanli Cheng Wei Dai Wen Chen Hua Xue Zhengzheng Zhao Zhengbing Jiang Huanan Li Jiashu Liu Feng Huang Minmin Cai Longyu Zheng Ziniu Yu Donghai Peng Jibin Zhang |
| author_sort | Wanli Cheng |
| collection | DOAJ |
| description | Furfural acetone (FAc) is widely used as an additive by the food industry, as well as an intermediate in several fine chemical industries. Its nematicidal activity against the free-living model organism Caenorhabditis elegans and the parasitic nematode Meloidogyne incognita are well known, but its molecular mechanism of action remains unclear. To deep this subject, we performed 48-h lethal tests on eight nematode species, encompassing free-living, plant-parasitic, and animal-parasitic nematodes. Our results revealed that FAc possesses broad-spectrum nematicidal activity, with potent effects against parasitic nematodes such as Strongyloides stercoralis and M. incognita. In contrast, it exhibited weak activity against the free-living nematode C. elegans, suggesting its potential as a selective nematicide. Our investigation unveiled that FAc binds to the vacuolar H+-ATPase subunits VHA-12 and VHA-13, accelerating intestinal cell necrosis and leading to the death of C. elegans. It is the first discovery that VHA-12 and VHA-13 can serve as target proteins for triggering nematode cell necrosis. The interaction results indicated that FAc targets proteins VHA-12 and VHA-13 of different nematodes and confers broad-spectrum nematicidal activity. And the Spearman analysis results illustrated that the differential nematicidal activity of FAc against various nematodes is attributed to variations in the sequence and structure of the receptor proteins VHA-12 and VHA-13 among different nematode species. Our results illuminate the molecular mechanism underlying the differential toxicity of FAc to different nematodes, and provide valuable data for the comprehensive risk assessment of FAc release into the environment. |
| format | Article |
| id | doaj-art-e9ef41ab01d7430bbfca69a5f6bd2d9c |
| institution | Kabale University |
| issn | 0147-6513 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Ecotoxicology and Environmental Safety |
| spelling | doaj-art-e9ef41ab01d7430bbfca69a5f6bd2d9c2024-12-07T08:24:42ZengElsevierEcotoxicology and Environmental Safety0147-65132024-12-01288117407Nematodes exposed to furfural acetone exhibit a species-specific vacuolar H+-ATPase responseWanli Cheng0Wei Dai1Wen Chen2Hua Xue3Zhengzheng Zhao4Zhengbing Jiang5Huanan Li6Jiashu Liu7Feng Huang8Minmin Cai9Longyu Zheng10Ziniu Yu11Donghai Peng12Jibin Zhang13State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Science, Hubei University, Wuhan, Hubei 430062, China; National Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, ChinaNational Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, ChinaNational Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, ChinaNational Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, ChinaNational Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, ChinaState Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Science, Hubei University, Wuhan, Hubei 430062, ChinaState Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Science, Hubei University, Wuhan, Hubei 430062, ChinaState Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Science, Hubei University, Wuhan, Hubei 430062, ChinaNational Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, ChinaNational Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, ChinaNational Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, ChinaNational Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, ChinaNational Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, ChinaNational Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, China; Corresponding author at: National Key Laboratory of Agricultural Microbiology and National Engineering Research Center of Microbial Pesticides, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China.Furfural acetone (FAc) is widely used as an additive by the food industry, as well as an intermediate in several fine chemical industries. Its nematicidal activity against the free-living model organism Caenorhabditis elegans and the parasitic nematode Meloidogyne incognita are well known, but its molecular mechanism of action remains unclear. To deep this subject, we performed 48-h lethal tests on eight nematode species, encompassing free-living, plant-parasitic, and animal-parasitic nematodes. Our results revealed that FAc possesses broad-spectrum nematicidal activity, with potent effects against parasitic nematodes such as Strongyloides stercoralis and M. incognita. In contrast, it exhibited weak activity against the free-living nematode C. elegans, suggesting its potential as a selective nematicide. Our investigation unveiled that FAc binds to the vacuolar H+-ATPase subunits VHA-12 and VHA-13, accelerating intestinal cell necrosis and leading to the death of C. elegans. It is the first discovery that VHA-12 and VHA-13 can serve as target proteins for triggering nematode cell necrosis. The interaction results indicated that FAc targets proteins VHA-12 and VHA-13 of different nematodes and confers broad-spectrum nematicidal activity. And the Spearman analysis results illustrated that the differential nematicidal activity of FAc against various nematodes is attributed to variations in the sequence and structure of the receptor proteins VHA-12 and VHA-13 among different nematode species. Our results illuminate the molecular mechanism underlying the differential toxicity of FAc to different nematodes, and provide valuable data for the comprehensive risk assessment of FAc release into the environment.http://www.sciencedirect.com/science/article/pii/S0147651324014830Parasitic nematodesNematicidal activityPhysiological effectsIntestinal cell necrosisVHA-12 proteinVHA-13 protein |
| spellingShingle | Wanli Cheng Wei Dai Wen Chen Hua Xue Zhengzheng Zhao Zhengbing Jiang Huanan Li Jiashu Liu Feng Huang Minmin Cai Longyu Zheng Ziniu Yu Donghai Peng Jibin Zhang Nematodes exposed to furfural acetone exhibit a species-specific vacuolar H+-ATPase response Ecotoxicology and Environmental Safety Parasitic nematodes Nematicidal activity Physiological effects Intestinal cell necrosis VHA-12 protein VHA-13 protein |
| title | Nematodes exposed to furfural acetone exhibit a species-specific vacuolar H+-ATPase response |
| title_full | Nematodes exposed to furfural acetone exhibit a species-specific vacuolar H+-ATPase response |
| title_fullStr | Nematodes exposed to furfural acetone exhibit a species-specific vacuolar H+-ATPase response |
| title_full_unstemmed | Nematodes exposed to furfural acetone exhibit a species-specific vacuolar H+-ATPase response |
| title_short | Nematodes exposed to furfural acetone exhibit a species-specific vacuolar H+-ATPase response |
| title_sort | nematodes exposed to furfural acetone exhibit a species specific vacuolar h atpase response |
| topic | Parasitic nematodes Nematicidal activity Physiological effects Intestinal cell necrosis VHA-12 protein VHA-13 protein |
| url | http://www.sciencedirect.com/science/article/pii/S0147651324014830 |
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