Unveiling a Virulence-Regulating Mechanism in Aeromonas hydrophila: a Quantitative Exoproteomic Analysis of an AraC-Like Protein
Bacterial AraC is a transcription factor family that initiates transcription by recruiting RNA polymerase to the promoter and directly regulating various bacterial phenotypes. It also directly regulates various bacterial phenotypes. However, how this transcription factor regulates bacterial virulenc...
| Main Authors: | , , , , , |
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| Format: | Article |
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Frontiers Media S.A.
2023-05-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1191209/full |
| _version_ | 1797830977004765184 |
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| author | Lishan Zhang Lishan Zhang Lina Sun Lina Sun Lina Sun Ramanathan Srinivasan Ramanathan Srinivasan Meizhen Lin Meizhen Lin Lanqing Gong Lanqing Gong Xiangmin Lin Xiangmin Lin |
| author_facet | Lishan Zhang Lishan Zhang Lina Sun Lina Sun Lina Sun Ramanathan Srinivasan Ramanathan Srinivasan Meizhen Lin Meizhen Lin Lanqing Gong Lanqing Gong Xiangmin Lin Xiangmin Lin |
| author_sort | Lishan Zhang |
| collection | DOAJ |
| description | Bacterial AraC is a transcription factor family that initiates transcription by recruiting RNA polymerase to the promoter and directly regulating various bacterial phenotypes. It also directly regulates various bacterial phenotypes. However, how this transcription factor regulates bacterial virulence and affects host immunity is still largely unknown. In this study, deleting the orf02889 (AraC-like transcription factor) gene in virulent Aeromonas hydrophila LP-2 affected several important phenotypes, such as increasing biofilm formation and siderophore production abilities. Moreover, Δorf02889 also significantly decreased the virulence of A. hydrophila and has promising attenuated vaccine potential. To better understand the effects of orf02889 on biological functions, a data independent acquisition (DIA)-based quantitative proteomics method was performed to compare the differentially expressed proteins between Δorf02889 and the wild-type strain in extracellular fractions. The following bioinformatics analysis suggested that ORF02889 may regulate various metabolic pathways, such as quorum sensing and ATP binding cassette (ABC) transporter metabolism. Moreover, 10 selected genes from the top 10 decreasing abundances in proteomics data were deleted, and their virulence to zebrafish was evaluated, respectively. The results showed that ΔcorC, Δorf00906, and Δorf04042 significantly reduced bacterial virulence. Finally, the following chromatin immunoprecipitation and polymerase chain reaction (ChIP-PCR) assay validated that the promoter of corC was directly regulated by ORF02889. Overall, these results provide insight into the biological function of ORF02889 and demonstrate its inherent regulatory mechanism for the virulence of A. hydrophila. |
| first_indexed | 2024-04-09T13:45:20Z |
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| id | doaj.art-8948f764b4f44da88bd2fe0730a613c7 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-09T13:45:20Z |
| publishDate | 2023-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-8948f764b4f44da88bd2fe0730a613c72023-05-09T05:13:55ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-05-011410.3389/fimmu.2023.11912091191209Unveiling a Virulence-Regulating Mechanism in Aeromonas hydrophila: a Quantitative Exoproteomic Analysis of an AraC-Like ProteinLishan Zhang0Lishan Zhang1Lina Sun2Lina Sun3Lina Sun4Ramanathan Srinivasan5Ramanathan Srinivasan6Meizhen Lin7Meizhen Lin8Lanqing Gong9Lanqing Gong10Xiangmin Lin11Xiangmin Lin12Fujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring (School of Life Sciences, Fujian Agriculture and Forestry University), Fuzhou, ChinaKey Laboratory of Crop Ecology and Molecular Physiology (Fujian Agriculture and Forestry University), Fujian Province University, Fuzhou, ChinaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring (School of Life Sciences, Fujian Agriculture and Forestry University), Fuzhou, ChinaKey Laboratory of Crop Ecology and Molecular Physiology (Fujian Agriculture and Forestry University), Fujian Province University, Fuzhou, ChinaState Key Laboratory of Microbial Technology, Shandong University, Qingdao, ChinaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring (School of Life Sciences, Fujian Agriculture and Forestry University), Fuzhou, ChinaCentre for Research, Centre for Materials Engineering and Regenerative Medicine, Bharath Institute of Higher Education and Research, Selaiyur, Chennai, Tamil Nadu, IndiaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring (School of Life Sciences, Fujian Agriculture and Forestry University), Fuzhou, ChinaKey Laboratory of Crop Ecology and Molecular Physiology (Fujian Agriculture and Forestry University), Fujian Province University, Fuzhou, ChinaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring (School of Life Sciences, Fujian Agriculture and Forestry University), Fuzhou, ChinaKey Laboratory of Crop Ecology and Molecular Physiology (Fujian Agriculture and Forestry University), Fujian Province University, Fuzhou, ChinaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring (School of Life Sciences, Fujian Agriculture and Forestry University), Fuzhou, ChinaKey Laboratory of Crop Ecology and Molecular Physiology (Fujian Agriculture and Forestry University), Fujian Province University, Fuzhou, ChinaBacterial AraC is a transcription factor family that initiates transcription by recruiting RNA polymerase to the promoter and directly regulating various bacterial phenotypes. It also directly regulates various bacterial phenotypes. However, how this transcription factor regulates bacterial virulence and affects host immunity is still largely unknown. In this study, deleting the orf02889 (AraC-like transcription factor) gene in virulent Aeromonas hydrophila LP-2 affected several important phenotypes, such as increasing biofilm formation and siderophore production abilities. Moreover, Δorf02889 also significantly decreased the virulence of A. hydrophila and has promising attenuated vaccine potential. To better understand the effects of orf02889 on biological functions, a data independent acquisition (DIA)-based quantitative proteomics method was performed to compare the differentially expressed proteins between Δorf02889 and the wild-type strain in extracellular fractions. The following bioinformatics analysis suggested that ORF02889 may regulate various metabolic pathways, such as quorum sensing and ATP binding cassette (ABC) transporter metabolism. Moreover, 10 selected genes from the top 10 decreasing abundances in proteomics data were deleted, and their virulence to zebrafish was evaluated, respectively. The results showed that ΔcorC, Δorf00906, and Δorf04042 significantly reduced bacterial virulence. Finally, the following chromatin immunoprecipitation and polymerase chain reaction (ChIP-PCR) assay validated that the promoter of corC was directly regulated by ORF02889. Overall, these results provide insight into the biological function of ORF02889 and demonstrate its inherent regulatory mechanism for the virulence of A. hydrophila.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1191209/fullAraC-like transcription factorquantitative proteomicsAeromonas hydrophilavirulenceORF02889 |
| spellingShingle | Lishan Zhang Lishan Zhang Lina Sun Lina Sun Lina Sun Ramanathan Srinivasan Ramanathan Srinivasan Meizhen Lin Meizhen Lin Lanqing Gong Lanqing Gong Xiangmin Lin Xiangmin Lin Unveiling a Virulence-Regulating Mechanism in Aeromonas hydrophila: a Quantitative Exoproteomic Analysis of an AraC-Like Protein Frontiers in Immunology AraC-like transcription factor quantitative proteomics Aeromonas hydrophila virulence ORF02889 |
| title | Unveiling a Virulence-Regulating Mechanism in Aeromonas hydrophila: a Quantitative Exoproteomic Analysis of an AraC-Like Protein |
| title_full | Unveiling a Virulence-Regulating Mechanism in Aeromonas hydrophila: a Quantitative Exoproteomic Analysis of an AraC-Like Protein |
| title_fullStr | Unveiling a Virulence-Regulating Mechanism in Aeromonas hydrophila: a Quantitative Exoproteomic Analysis of an AraC-Like Protein |
| title_full_unstemmed | Unveiling a Virulence-Regulating Mechanism in Aeromonas hydrophila: a Quantitative Exoproteomic Analysis of an AraC-Like Protein |
| title_short | Unveiling a Virulence-Regulating Mechanism in Aeromonas hydrophila: a Quantitative Exoproteomic Analysis of an AraC-Like Protein |
| title_sort | unveiling a virulence regulating mechanism in aeromonas hydrophila a quantitative exoproteomic analysis of an arac like protein |
| topic | AraC-like transcription factor quantitative proteomics Aeromonas hydrophila virulence ORF02889 |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1191209/full |
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