Hosts and Commensal Bacteria Synergistically Antagonize Opportunistic Pathogens at the Single‐Cell Resolution
Abstract Natural microbes coexist in a diverse species population with competition for space and nutrient resources. However, the molecular mechanisms underpinning the regulatory networks of microbes among themselves and with their host are still in infancy. Here, it is reported that Drosophila and...
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Wiley
2025-08-01
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| Series: | Advanced Science |
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| Online Access: | https://doi.org/10.1002/advs.202500582 |
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| author | Sheng Zhang Ziguang Wang Anqi Liu Jinshu Li Jingjing Zhuang Xiaowen Ji Paul I. Mulama Maoye Li Haiqun Cao Eng‐King Tan Wei Liu |
| author_facet | Sheng Zhang Ziguang Wang Anqi Liu Jinshu Li Jingjing Zhuang Xiaowen Ji Paul I. Mulama Maoye Li Haiqun Cao Eng‐King Tan Wei Liu |
| author_sort | Sheng Zhang |
| collection | DOAJ |
| description | Abstract Natural microbes coexist in a diverse species population with competition for space and nutrient resources. However, the molecular mechanisms underpinning the regulatory networks of microbes among themselves and with their host are still in infancy. Here, it is reported that Drosophila and the commensal Lactiplantibacillus plantarum form an alliance to compete with the pathogenic Serratia marcescens using the integrated three‐species model system. In the dual‐species model, larvae diminish the L. plantarum population, but reversibly increase lactate production through altering its transcriptional reprogramming. In the tripartite‐species model, larvae facilitate the growth of L. plantarum that confers colonization resistance against S. marcescens. On the other hand, S. marcescens launches sophisticated arms race strategies to impair colonization resistance by sensing lactate derived from L. plantarum. More importantly, the S. marcescens population challenged with Drosophila and L. plantarum adaptively diverge into virulent and reduced virulence subclusters with an increase in resistance heterogeneity. To form the alliance with Drosophila, heterogeneity in lactate generation is broadened among L. plantarum subpopulations. Altogether, these findings provide an insight into the host‐commensal‐pathogen symbiosis at both bulk and single‐cell resolutions, advancing fundamental concepts of precise manipulation of bacterial communities. |
| format | Article |
| id | doaj-art-65e94dd752114a4b9c54d71ca8bd7006 |
| institution | Kabale University |
| issn | 2198-3844 |
| language | English |
| publishDate | 2025-08-01 |
| publisher | Wiley |
| record_format | Article |
| series | Advanced Science |
| spelling | doaj-art-65e94dd752114a4b9c54d71ca8bd70062025-08-20T11:56:10ZengWileyAdvanced Science2198-38442025-08-011230n/an/a10.1002/advs.202500582Hosts and Commensal Bacteria Synergistically Antagonize Opportunistic Pathogens at the Single‐Cell ResolutionSheng Zhang0Ziguang Wang1Anqi Liu2Jinshu Li3Jingjing Zhuang4Xiaowen Ji5Paul I. Mulama6Maoye Li7Haiqun Cao8Eng‐King Tan9Wei Liu10School of Plant Protection Anhui Agricultural University Anhui Province Key Laboratory of Crop Integrated Pest Management Anhui Province Key Laboratory of Resource Insect Biology and Innovative Utilization Hefei 230036 ChinaCollege of Life Sciences Nankai University Tianjin 300071 ChinaSchool of Plant Protection Anhui Agricultural University Anhui Province Key Laboratory of Crop Integrated Pest Management Anhui Province Key Laboratory of Resource Insect Biology and Innovative Utilization Hefei 230036 ChinaSchool of Plant Protection Anhui Agricultural University Anhui Province Key Laboratory of Crop Integrated Pest Management Anhui Province Key Laboratory of Resource Insect Biology and Innovative Utilization Hefei 230036 ChinaSchool of Plant Protection Anhui Agricultural University Anhui Province Key Laboratory of Crop Integrated Pest Management Anhui Province Key Laboratory of Resource Insect Biology and Innovative Utilization Hefei 230036 ChinaSchool of Plant Protection Anhui Agricultural University Anhui Province Key Laboratory of Crop Integrated Pest Management Anhui Province Key Laboratory of Resource Insect Biology and Innovative Utilization Hefei 230036 ChinaSchool of Plant Protection Anhui Agricultural University Anhui Province Key Laboratory of Crop Integrated Pest Management Anhui Province Key Laboratory of Resource Insect Biology and Innovative Utilization Hefei 230036 ChinaSchool of Plant Protection Anhui Agricultural University Anhui Province Key Laboratory of Crop Integrated Pest Management Anhui Province Key Laboratory of Resource Insect Biology and Innovative Utilization Hefei 230036 ChinaSchool of Plant Protection Anhui Agricultural University Anhui Province Key Laboratory of Crop Integrated Pest Management Anhui Province Key Laboratory of Resource Insect Biology and Innovative Utilization Hefei 230036 ChinaDepartment of Neurology National Neuroscience Institute Singapore 308433 SingaporeSchool of Plant Protection Anhui Agricultural University Anhui Province Key Laboratory of Crop Integrated Pest Management Anhui Province Key Laboratory of Resource Insect Biology and Innovative Utilization Hefei 230036 ChinaAbstract Natural microbes coexist in a diverse species population with competition for space and nutrient resources. However, the molecular mechanisms underpinning the regulatory networks of microbes among themselves and with their host are still in infancy. Here, it is reported that Drosophila and the commensal Lactiplantibacillus plantarum form an alliance to compete with the pathogenic Serratia marcescens using the integrated three‐species model system. In the dual‐species model, larvae diminish the L. plantarum population, but reversibly increase lactate production through altering its transcriptional reprogramming. In the tripartite‐species model, larvae facilitate the growth of L. plantarum that confers colonization resistance against S. marcescens. On the other hand, S. marcescens launches sophisticated arms race strategies to impair colonization resistance by sensing lactate derived from L. plantarum. More importantly, the S. marcescens population challenged with Drosophila and L. plantarum adaptively diverge into virulent and reduced virulence subclusters with an increase in resistance heterogeneity. To form the alliance with Drosophila, heterogeneity in lactate generation is broadened among L. plantarum subpopulations. Altogether, these findings provide an insight into the host‐commensal‐pathogen symbiosis at both bulk and single‐cell resolutions, advancing fundamental concepts of precise manipulation of bacterial communities.https://doi.org/10.1002/advs.202500582bacterial single‐cell RNA‐seqheterogeneitymetabolic adaptationspathogenicity |
| spellingShingle | Sheng Zhang Ziguang Wang Anqi Liu Jinshu Li Jingjing Zhuang Xiaowen Ji Paul I. Mulama Maoye Li Haiqun Cao Eng‐King Tan Wei Liu Hosts and Commensal Bacteria Synergistically Antagonize Opportunistic Pathogens at the Single‐Cell Resolution Advanced Science bacterial single‐cell RNA‐seq heterogeneity metabolic adaptations pathogenicity |
| title | Hosts and Commensal Bacteria Synergistically Antagonize Opportunistic Pathogens at the Single‐Cell Resolution |
| title_full | Hosts and Commensal Bacteria Synergistically Antagonize Opportunistic Pathogens at the Single‐Cell Resolution |
| title_fullStr | Hosts and Commensal Bacteria Synergistically Antagonize Opportunistic Pathogens at the Single‐Cell Resolution |
| title_full_unstemmed | Hosts and Commensal Bacteria Synergistically Antagonize Opportunistic Pathogens at the Single‐Cell Resolution |
| title_short | Hosts and Commensal Bacteria Synergistically Antagonize Opportunistic Pathogens at the Single‐Cell Resolution |
| title_sort | hosts and commensal bacteria synergistically antagonize opportunistic pathogens at the single cell resolution |
| topic | bacterial single‐cell RNA‐seq heterogeneity metabolic adaptations pathogenicity |
| url | https://doi.org/10.1002/advs.202500582 |
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