Phage‐mediated horizontal transfer of Salmonella enterica virulence genes with regulatory feedback from the host
Abstract Phage‐mediated horizontal transfer of virulence genes can enhance the transmission and pathogenicity of Salmonella enterica (S. enterica), a process potentially regulated by its regulatory mechanisms. In this study, we explored the global dynamics of phage‐mediated horizontal transfer in S....
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Wiley
2025-08-01
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| Online Access: | https://doi.org/10.1002/imt2.70042 |
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| author | Tianjing She Demeng Tan Jose Luis Balcazar Ville‐Petri Friman Danrui Wang Dong Zhu Mao Ye Mingming Sun Shujian Yuan Feng Hu |
| author_facet | Tianjing She Demeng Tan Jose Luis Balcazar Ville‐Petri Friman Danrui Wang Dong Zhu Mao Ye Mingming Sun Shujian Yuan Feng Hu |
| author_sort | Tianjing She |
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| description | Abstract Phage‐mediated horizontal transfer of virulence genes can enhance the transmission and pathogenicity of Salmonella enterica (S. enterica), a process potentially regulated by its regulatory mechanisms. In this study, we explored the global dynamics of phage‐mediated horizontal transfer in S. enterica and investigated the role of its regulatory mechanisms in transduction. A total of 5178 viral sequences encoding 12 S. enterica virulence genes were retrieved from the Integrated Microbial Genomes and Virome (IMG/VR) database, alongside 466,136 S. enterica genomes from EnteroBase. Virulence genes, including iacP (acyl carrier protein), mgtB (P‐type Mg2+ transporter), misL (autotransporter porin), and fliC (flagellar filament protein), were widely distributed in phages and S. enterica across North America, Europe, and Asia. Phylogenetic analysis revealed close genetic affinity between phage‐ and bacterial‐encoded virulence genes, suggesting shared ancestry and historical horizontal gene transfer events. The global regulator carbon storage regulator A (csrA) was highly conserved and ubiquitous in S. enterica. Overexpression of csrA inhibited prophage cyclization and release by upregulating the prophage cI repressor during horizontal gene transfer. Overall, these findings enhance our understanding of phage‐mediated horizontal transfer of virulence genes, explore new areas of bacterial regulators that inhibit gene exchange and evolution by affecting phage life cycles, and offer a novel approach to controlling the transmission of phage‐mediated S. enterica virulence genes. |
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| institution | Kabale University |
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| language | English |
| publishDate | 2025-08-01 |
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| spelling | doaj-art-6422569af2264ac79bd1bd59258cccb72025-08-22T08:13:03ZengWileyiMeta2770-596X2025-08-0144n/an/a10.1002/imt2.70042Phage‐mediated horizontal transfer of Salmonella enterica virulence genes with regulatory feedback from the hostTianjing She0Demeng Tan1Jose Luis Balcazar2Ville‐Petri Friman3Danrui Wang4Dong Zhu5Mao Ye6Mingming Sun7Shujian Yuan8Feng Hu9Soil Ecology Lab, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization and Jiangsu Key Laboratory for Solid Organic Waste Utilization Nanjing Agricultural University Nanjing ChinaShanghai Public Health Clinical Center Fudan University Shanghai ChinaCatalan Institute for Water Research ICRA Girona SpainDepartment of Microbiology University of Helsinki Helsinki FinlandSoil Ecology Lab, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization and Jiangsu Key Laboratory for Solid Organic Waste Utilization Nanjing Agricultural University Nanjing ChinaZhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, Ningbo Urban Environment Observation and Research Station Chinese Academy of Sciences Ningbo ChinaNational Engineering Research Center for Soil Nutrient Management and Pollution Remediation, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaSoil Ecology Lab, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization and Jiangsu Key Laboratory for Solid Organic Waste Utilization Nanjing Agricultural University Nanjing ChinaSoil Ecology Lab, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization and Jiangsu Key Laboratory for Solid Organic Waste Utilization Nanjing Agricultural University Nanjing ChinaSoil Ecology Lab, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization and Jiangsu Key Laboratory for Solid Organic Waste Utilization Nanjing Agricultural University Nanjing ChinaAbstract Phage‐mediated horizontal transfer of virulence genes can enhance the transmission and pathogenicity of Salmonella enterica (S. enterica), a process potentially regulated by its regulatory mechanisms. In this study, we explored the global dynamics of phage‐mediated horizontal transfer in S. enterica and investigated the role of its regulatory mechanisms in transduction. A total of 5178 viral sequences encoding 12 S. enterica virulence genes were retrieved from the Integrated Microbial Genomes and Virome (IMG/VR) database, alongside 466,136 S. enterica genomes from EnteroBase. Virulence genes, including iacP (acyl carrier protein), mgtB (P‐type Mg2+ transporter), misL (autotransporter porin), and fliC (flagellar filament protein), were widely distributed in phages and S. enterica across North America, Europe, and Asia. Phylogenetic analysis revealed close genetic affinity between phage‐ and bacterial‐encoded virulence genes, suggesting shared ancestry and historical horizontal gene transfer events. The global regulator carbon storage regulator A (csrA) was highly conserved and ubiquitous in S. enterica. Overexpression of csrA inhibited prophage cyclization and release by upregulating the prophage cI repressor during horizontal gene transfer. Overall, these findings enhance our understanding of phage‐mediated horizontal transfer of virulence genes, explore new areas of bacterial regulators that inhibit gene exchange and evolution by affecting phage life cycles, and offer a novel approach to controlling the transmission of phage‐mediated S. enterica virulence genes.https://doi.org/10.1002/imt2.70042horizontal gene transferphagesregulatorsSalmonella entericavirulence genes |
| spellingShingle | Tianjing She Demeng Tan Jose Luis Balcazar Ville‐Petri Friman Danrui Wang Dong Zhu Mao Ye Mingming Sun Shujian Yuan Feng Hu Phage‐mediated horizontal transfer of Salmonella enterica virulence genes with regulatory feedback from the host iMeta horizontal gene transfer phages regulators Salmonella enterica virulence genes |
| title | Phage‐mediated horizontal transfer of Salmonella enterica virulence genes with regulatory feedback from the host |
| title_full | Phage‐mediated horizontal transfer of Salmonella enterica virulence genes with regulatory feedback from the host |
| title_fullStr | Phage‐mediated horizontal transfer of Salmonella enterica virulence genes with regulatory feedback from the host |
| title_full_unstemmed | Phage‐mediated horizontal transfer of Salmonella enterica virulence genes with regulatory feedback from the host |
| title_short | Phage‐mediated horizontal transfer of Salmonella enterica virulence genes with regulatory feedback from the host |
| title_sort | phage mediated horizontal transfer of salmonella enterica virulence genes with regulatory feedback from the host |
| topic | horizontal gene transfer phages regulators Salmonella enterica virulence genes |
| url | https://doi.org/10.1002/imt2.70042 |
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