Single-cell transcriptomics unveils leukocyte heterogeneity in the gills of Larimichthys crocea in response to parasitic infection
BackgroundFish gills serve as critical immune interfaces against aquatic pathogens, yet their leukocyte heterogeneity in response to parasitic infections remains poorly understood.MethodsSingle-cell RNA sequencing was employed to elucidate leukocyte responses in the gills of Larimichthys crocea duri...
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Frontiers Media S.A.
2025-08-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2025.1633701/full |
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| author | Qiuhua Li Qiuhua Li Meiyan Wang Chenhao Li Ngoc Tuan Tran Jingqun Ao Shengkang Li Xinhua Chen |
| author_facet | Qiuhua Li Qiuhua Li Meiyan Wang Chenhao Li Ngoc Tuan Tran Jingqun Ao Shengkang Li Xinhua Chen |
| author_sort | Qiuhua Li |
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| description | BackgroundFish gills serve as critical immune interfaces against aquatic pathogens, yet their leukocyte heterogeneity in response to parasitic infections remains poorly understood.MethodsSingle-cell RNA sequencing was employed to elucidate leukocyte responses in the gills of Larimichthys crocea during Cryptocaryon irritans infection.ResultsA total of 13,070 leukocytes from the gills under steady-state and infected conditions were profiled and classified into eight principal lineages: T cells (> 70% of total immune cells), ILC2-like cells, NK-like cells, neutrophils, cpa5+ granulocytes, B cells, macrophages, and dendritic cells. Following infection, T cell subsets exhibited distinct responses: Regulatory T cells expanded and demonstrated immunoregulatory capacity; CD8+ T cells exhibited cytotoxic responses; CD4-CD8- T cells displayed Th17-like functions; and γδ T cells showed Th2-like activity. ILC2-like cells significantly increased in abundance and upregulated type 2 cytokine expression, whereas cytotoxic NK-like cells enhanced chemokine signaling and cytotoxicity. Neutrophils increased in number and oxidative activity, while cpa5+ granulocytes highlighted immunomodulatory functions. Macrophages, dendritic cells, and B cells exhibited compartmentalized activation states, upregulating gene modules associated with pathogen recognition, antigen processing/presentation, chemotactic activity, and antibody defenses.ConclusionsThese findings describe a multi-layered immune cell defense strategy in the gills of teleosts against parasitic infection, showing conserved and fish-specific adaptations. Understanding gill immunity provides viable targets for enhancing parasite resistance in aquaculture, such as modulating ILC2/Treg pathways to prevent infections. |
| format | Article |
| id | doaj-art-9a4fc4c1910c46948cb28461bf64ffa8 |
| institution | Kabale University |
| issn | 1664-3224 |
| language | English |
| publishDate | 2025-08-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Immunology |
| spelling | doaj-art-9a4fc4c1910c46948cb28461bf64ffa82025-08-20T03:32:08ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-08-011610.3389/fimmu.2025.16337011633701Single-cell transcriptomics unveils leukocyte heterogeneity in the gills of Larimichthys crocea in response to parasitic infectionQiuhua Li0Qiuhua Li1Meiyan Wang2Chenhao Li3Ngoc Tuan Tran4Jingqun Ao5Shengkang Li6Xinhua Chen7Guangdong Provincial Key Laboratory of Marine Biology, Shantou University, Shantou, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaGuangdong Provincial Key Laboratory of Marine Biology, Shantou University, Shantou, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaGuangdong Provincial Key Laboratory of Marine Biology, Shantou University, Shantou, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaBackgroundFish gills serve as critical immune interfaces against aquatic pathogens, yet their leukocyte heterogeneity in response to parasitic infections remains poorly understood.MethodsSingle-cell RNA sequencing was employed to elucidate leukocyte responses in the gills of Larimichthys crocea during Cryptocaryon irritans infection.ResultsA total of 13,070 leukocytes from the gills under steady-state and infected conditions were profiled and classified into eight principal lineages: T cells (> 70% of total immune cells), ILC2-like cells, NK-like cells, neutrophils, cpa5+ granulocytes, B cells, macrophages, and dendritic cells. Following infection, T cell subsets exhibited distinct responses: Regulatory T cells expanded and demonstrated immunoregulatory capacity; CD8+ T cells exhibited cytotoxic responses; CD4-CD8- T cells displayed Th17-like functions; and γδ T cells showed Th2-like activity. ILC2-like cells significantly increased in abundance and upregulated type 2 cytokine expression, whereas cytotoxic NK-like cells enhanced chemokine signaling and cytotoxicity. Neutrophils increased in number and oxidative activity, while cpa5+ granulocytes highlighted immunomodulatory functions. Macrophages, dendritic cells, and B cells exhibited compartmentalized activation states, upregulating gene modules associated with pathogen recognition, antigen processing/presentation, chemotactic activity, and antibody defenses.ConclusionsThese findings describe a multi-layered immune cell defense strategy in the gills of teleosts against parasitic infection, showing conserved and fish-specific adaptations. Understanding gill immunity provides viable targets for enhancing parasite resistance in aquaculture, such as modulating ILC2/Treg pathways to prevent infections.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1633701/fullgill immunityLarimichthys croceasingle-cell transcriptomicsCryptocaryon irritansimmune cell heterogeneity |
| spellingShingle | Qiuhua Li Qiuhua Li Meiyan Wang Chenhao Li Ngoc Tuan Tran Jingqun Ao Shengkang Li Xinhua Chen Single-cell transcriptomics unveils leukocyte heterogeneity in the gills of Larimichthys crocea in response to parasitic infection Frontiers in Immunology gill immunity Larimichthys crocea single-cell transcriptomics Cryptocaryon irritans immune cell heterogeneity |
| title | Single-cell transcriptomics unveils leukocyte heterogeneity in the gills of Larimichthys crocea in response to parasitic infection |
| title_full | Single-cell transcriptomics unveils leukocyte heterogeneity in the gills of Larimichthys crocea in response to parasitic infection |
| title_fullStr | Single-cell transcriptomics unveils leukocyte heterogeneity in the gills of Larimichthys crocea in response to parasitic infection |
| title_full_unstemmed | Single-cell transcriptomics unveils leukocyte heterogeneity in the gills of Larimichthys crocea in response to parasitic infection |
| title_short | Single-cell transcriptomics unveils leukocyte heterogeneity in the gills of Larimichthys crocea in response to parasitic infection |
| title_sort | single cell transcriptomics unveils leukocyte heterogeneity in the gills of larimichthys crocea in response to parasitic infection |
| topic | gill immunity Larimichthys crocea single-cell transcriptomics Cryptocaryon irritans immune cell heterogeneity |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2025.1633701/full |
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