Roles of SPI-2 T3SS effectors in virulence of Salmonella Choleraesuis and Construction of a triple-gene mutant vaccine strain
Effector protein functions of Type III secretion system (T3SS) encoded by Salmonella pathogenicity islands 2 (SPI-2) have not been fully characterized in Salmonella enterica serovar Choleraesuis. This study characterized 21 effectors of SPI-2 T3SS of S. Choleraesuis in terms of macrophage survival a...
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Frontiers Media S.A.
2025-08-01
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| author | Rui Xu Rui Xu Rui Xu Rui Xu Xiangfei Ji Xiangfei Ji Xiangfei Ji Xiangfei Ji Junqi Lian Dekang Zhu Dekang Zhu Dekang Zhu Dekang Zhu Mafeng Liu Mafeng Liu Mafeng Liu Mafeng Liu Mingshu Wang Mingshu Wang Mingshu Wang Mingshu Wang Renyong Jia Renyong Jia Renyong Jia Renyong Jia Shun Chen Shun Chen Shun Chen Shun Chen Qiao Yang Qiao Yang Qiao Yang Qiao Yang Ying Wu Ying Wu Ying Wu Ying Wu Shaqiu Zhang Shaqiu Zhang Shaqiu Zhang Shaqiu Zhang Juan Huang Juan Huang Juan Huang Juan Huang Xumin Ou Xumin Ou Xumin Ou Xumin Ou Di Sun Di Sun Di Sun Di Sun Bin Tian Bin Tian Bin Tian Bin Tian Yu He Yu He Yu He Yu He Zhen Wu Zhen Wu Zhen Wu Zhen Wu Anchun Cheng Anchun Cheng Anchun Cheng Anchun Cheng Xinxin Zhao Xinxin Zhao Xinxin Zhao Xinxin Zhao |
| author_facet | Rui Xu Rui Xu Rui Xu Rui Xu Xiangfei Ji Xiangfei Ji Xiangfei Ji Xiangfei Ji Junqi Lian Dekang Zhu Dekang Zhu Dekang Zhu Dekang Zhu Mafeng Liu Mafeng Liu Mafeng Liu Mafeng Liu Mingshu Wang Mingshu Wang Mingshu Wang Mingshu Wang Renyong Jia Renyong Jia Renyong Jia Renyong Jia Shun Chen Shun Chen Shun Chen Shun Chen Qiao Yang Qiao Yang Qiao Yang Qiao Yang Ying Wu Ying Wu Ying Wu Ying Wu Shaqiu Zhang Shaqiu Zhang Shaqiu Zhang Shaqiu Zhang Juan Huang Juan Huang Juan Huang Juan Huang Xumin Ou Xumin Ou Xumin Ou Xumin Ou Di Sun Di Sun Di Sun Di Sun Bin Tian Bin Tian Bin Tian Bin Tian Yu He Yu He Yu He Yu He Zhen Wu Zhen Wu Zhen Wu Zhen Wu Anchun Cheng Anchun Cheng Anchun Cheng Anchun Cheng Xinxin Zhao Xinxin Zhao Xinxin Zhao Xinxin Zhao |
| author_sort | Rui Xu |
| collection | DOAJ |
| description | Effector protein functions of Type III secretion system (T3SS) encoded by Salmonella pathogenicity islands 2 (SPI-2) have not been fully characterized in Salmonella enterica serovar Choleraesuis. This study characterized 21 effectors of SPI-2 T3SS of S. Choleraesuis in terms of macrophage survival and virulence in mice via construction of various gene mutant strains. Eight effector genes including sseF, sseJ, sifB, sseK, sifA, sopD2, steC, and steD contributed to bacterial survival in macrophage cell line RAW264.7; whereas only sopD2 also promoted bacterial virulence in mice like other three effector genes sseL, steA, and spiC. The mutant strain, ΔsopD2, ΔsseL, ΔsteA, or ΔspiC, led to higher mouse survival compared to the wild-type strain post-oral infection, while their bacterial loads in spleen and liver were not reduced except the ΔspiC that was undetectable in mouse tissues. Then, the triple-gene mutant strain ΔsseLΔsopD2ΔsteA was constructed and found to be virulence attenuated with a compromised colonization ability. Finally, immunization of this mutant orally induced robust serum IgG responses and provided 40% protection against lethal S. Choleraesuis challenge. Our study highlights the critical role of four SPI-2 T3SS effectors in S. Choleraesuis pathogenesis. |
| format | Article |
| id | doaj-art-2f3ed0280c4748f2a8e6af09e65a7edb |
| institution | Kabale University |
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| language | English |
| publishDate | 2025-08-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Veterinary Science |
| spelling | doaj-art-2f3ed0280c4748f2a8e6af09e65a7edb2025-08-20T03:35:57ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692025-08-011210.3389/fvets.2025.16373271637327Roles of SPI-2 T3SS effectors in virulence of Salmonella Choleraesuis and Construction of a triple-gene mutant vaccine strainRui Xu0Rui Xu1Rui Xu2Rui Xu3Xiangfei Ji4Xiangfei Ji5Xiangfei Ji6Xiangfei Ji7Junqi Lian8Dekang Zhu9Dekang Zhu10Dekang Zhu11Dekang Zhu12Mafeng Liu13Mafeng Liu14Mafeng Liu15Mafeng Liu16Mingshu Wang17Mingshu Wang18Mingshu Wang19Mingshu Wang20Renyong Jia21Renyong Jia22Renyong Jia23Renyong Jia24Shun Chen25Shun Chen26Shun Chen27Shun Chen28Qiao Yang29Qiao Yang30Qiao Yang31Qiao Yang32Ying Wu33Ying Wu34Ying Wu35Ying Wu36Shaqiu Zhang37Shaqiu Zhang38Shaqiu Zhang39Shaqiu Zhang40Juan Huang41Juan Huang42Juan Huang43Juan Huang44Xumin Ou45Xumin Ou46Xumin Ou47Xumin Ou48Di Sun49Di Sun50Di Sun51Di Sun52Bin Tian53Bin Tian54Bin Tian55Bin Tian56Yu He57Yu He58Yu He59Yu He60Zhen Wu61Zhen Wu62Zhen Wu63Zhen Wu64Anchun Cheng65Anchun Cheng66Anchun Cheng67Anchun Cheng68Xinxin Zhao69Xinxin Zhao70Xinxin Zhao71Xinxin Zhao72Institute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaHulunbuir Agricultural and Livestock Product Quality and Safety Center, Hulunbuir, Inner Mongolia, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaInstitute of Veterinary Medicine and Immunology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaResearch Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaKey Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, ChinaEngineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the People's Republic of China, Chengdu, Sichuan, ChinaEffector protein functions of Type III secretion system (T3SS) encoded by Salmonella pathogenicity islands 2 (SPI-2) have not been fully characterized in Salmonella enterica serovar Choleraesuis. This study characterized 21 effectors of SPI-2 T3SS of S. Choleraesuis in terms of macrophage survival and virulence in mice via construction of various gene mutant strains. Eight effector genes including sseF, sseJ, sifB, sseK, sifA, sopD2, steC, and steD contributed to bacterial survival in macrophage cell line RAW264.7; whereas only sopD2 also promoted bacterial virulence in mice like other three effector genes sseL, steA, and spiC. The mutant strain, ΔsopD2, ΔsseL, ΔsteA, or ΔspiC, led to higher mouse survival compared to the wild-type strain post-oral infection, while their bacterial loads in spleen and liver were not reduced except the ΔspiC that was undetectable in mouse tissues. Then, the triple-gene mutant strain ΔsseLΔsopD2ΔsteA was constructed and found to be virulence attenuated with a compromised colonization ability. Finally, immunization of this mutant orally induced robust serum IgG responses and provided 40% protection against lethal S. Choleraesuis challenge. Our study highlights the critical role of four SPI-2 T3SS effectors in S. Choleraesuis pathogenesis.https://www.frontiersin.org/articles/10.3389/fvets.2025.1637327/fullS. choleraesuisSPI-2type III secretion systemvirulencevaccines |
| spellingShingle | Rui Xu Rui Xu Rui Xu Rui Xu Xiangfei Ji Xiangfei Ji Xiangfei Ji Xiangfei Ji Junqi Lian Dekang Zhu Dekang Zhu Dekang Zhu Dekang Zhu Mafeng Liu Mafeng Liu Mafeng Liu Mafeng Liu Mingshu Wang Mingshu Wang Mingshu Wang Mingshu Wang Renyong Jia Renyong Jia Renyong Jia Renyong Jia Shun Chen Shun Chen Shun Chen Shun Chen Qiao Yang Qiao Yang Qiao Yang Qiao Yang Ying Wu Ying Wu Ying Wu Ying Wu Shaqiu Zhang Shaqiu Zhang Shaqiu Zhang Shaqiu Zhang Juan Huang Juan Huang Juan Huang Juan Huang Xumin Ou Xumin Ou Xumin Ou Xumin Ou Di Sun Di Sun Di Sun Di Sun Bin Tian Bin Tian Bin Tian Bin Tian Yu He Yu He Yu He Yu He Zhen Wu Zhen Wu Zhen Wu Zhen Wu Anchun Cheng Anchun Cheng Anchun Cheng Anchun Cheng Xinxin Zhao Xinxin Zhao Xinxin Zhao Xinxin Zhao Roles of SPI-2 T3SS effectors in virulence of Salmonella Choleraesuis and Construction of a triple-gene mutant vaccine strain Frontiers in Veterinary Science S. choleraesuis SPI-2 type III secretion system virulence vaccines |
| title | Roles of SPI-2 T3SS effectors in virulence of Salmonella Choleraesuis and Construction of a triple-gene mutant vaccine strain |
| title_full | Roles of SPI-2 T3SS effectors in virulence of Salmonella Choleraesuis and Construction of a triple-gene mutant vaccine strain |
| title_fullStr | Roles of SPI-2 T3SS effectors in virulence of Salmonella Choleraesuis and Construction of a triple-gene mutant vaccine strain |
| title_full_unstemmed | Roles of SPI-2 T3SS effectors in virulence of Salmonella Choleraesuis and Construction of a triple-gene mutant vaccine strain |
| title_short | Roles of SPI-2 T3SS effectors in virulence of Salmonella Choleraesuis and Construction of a triple-gene mutant vaccine strain |
| title_sort | roles of spi 2 t3ss effectors in virulence of salmonella choleraesuis and construction of a triple gene mutant vaccine strain |
| topic | S. choleraesuis SPI-2 type III secretion system virulence vaccines |
| url | https://www.frontiersin.org/articles/10.3389/fvets.2025.1637327/full |
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