Integrated morphological and transcriptome profiles reveal a highly-developed extrusome system associated to virulence in the notorious fish parasite, Ichthyophthirius multifiliis
ABSTRACTIchthyophthirius multifiliis is an obligate parasitic ciliate that causes severe economic damage in aquaculture. The parasite contains numerous extrusive organelles (extrusomes) that assist in its pathogenesis and reproduction. However, the structure of these extrusomes and the molecular pro...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2023-12-01
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| Series: | Virulence |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/21505594.2023.2242622 |
| _version_ | 1797367141986467840 |
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| author | Hao Yang Zhe Wang Jieyin Xiao Jingbo Hu Xiao Tu Zemao Gu |
| author_facet | Hao Yang Zhe Wang Jieyin Xiao Jingbo Hu Xiao Tu Zemao Gu |
| author_sort | Hao Yang |
| collection | DOAJ |
| description | ABSTRACTIchthyophthirius multifiliis is an obligate parasitic ciliate that causes severe economic damage in aquaculture. The parasite contains numerous extrusive organelles (extrusomes) that assist in its pathogenesis and reproduction. However, the structure of these extrusomes and the molecular profiles involved in exocytosis remain unclear. In the present study, through comparative ultrastructural observations across the life cycle of I. multifiliis, we demonstrated that all three of its life stages (theront, trophont, and tomont) exhibited an abundance of extrusomes. In addition, two different types of extrusomes were identified according to their unique structures. Type I extrusomes (mucocysts) are crystalline, oval-shaped, 0.7–1.4 × 0.6–1.1 μm, and distributed as “rosettes” below the trophont membrane. Type II extrusomes, 2.0–3.0 × 0.2–0.3 μm, are rod-shaped with tubular cores and identified as toxicysts, the aggregation of which in the anterior part of the theront and cortex of the trophont revealed their potential roles in I. multifiliis invasion. This was confirmed by our transcriptome investigations of the three stages of I. multifiliis, which revealed that a set of genes involved in proteolysis and DNA/protein biogenesis was highly expressed in the theront and trophont. Furthermore, to map the molecular mechanisms of extrusome release, we characterized 25 Rab family genes in I. multifiliis and determined their expression profiles across the life cycle, reflecting the distribution patterns of the two extrusomes. Collectively, our data revealed that a highly developed extrusome system could play a potential role in the virulence of I. multifiliis, which facilitates a better understanding of the parasite’s development. |
| first_indexed | 2024-03-08T17:14:07Z |
| format | Article |
| id | doaj.art-a92efe794ca44efc875599f99751a560 |
| institution | Directory Open Access Journal |
| issn | 2150-5594 2150-5608 |
| language | English |
| last_indexed | 2024-03-08T17:14:07Z |
| publishDate | 2023-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Virulence |
| spelling | doaj.art-a92efe794ca44efc875599f99751a5602024-01-03T17:26:57ZengTaylor & Francis GroupVirulence2150-55942150-56082023-12-0114110.1080/21505594.2023.2242622Integrated morphological and transcriptome profiles reveal a highly-developed extrusome system associated to virulence in the notorious fish parasite, Ichthyophthirius multifiliisHao Yang0Zhe Wang1Jieyin Xiao2Jingbo Hu3Xiao Tu4Zemao Gu5College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaMarine College, Shandong University, Weihai, ChinaCollege of Fisheries, Huazhong Agricultural University, Wuhan, ChinaCollege of Fisheries, Huazhong Agricultural University, Wuhan, ChinaCollege of Fisheries, Huazhong Agricultural University, Wuhan, ChinaCollege of Fisheries, Huazhong Agricultural University, Wuhan, ChinaABSTRACTIchthyophthirius multifiliis is an obligate parasitic ciliate that causes severe economic damage in aquaculture. The parasite contains numerous extrusive organelles (extrusomes) that assist in its pathogenesis and reproduction. However, the structure of these extrusomes and the molecular profiles involved in exocytosis remain unclear. In the present study, through comparative ultrastructural observations across the life cycle of I. multifiliis, we demonstrated that all three of its life stages (theront, trophont, and tomont) exhibited an abundance of extrusomes. In addition, two different types of extrusomes were identified according to their unique structures. Type I extrusomes (mucocysts) are crystalline, oval-shaped, 0.7–1.4 × 0.6–1.1 μm, and distributed as “rosettes” below the trophont membrane. Type II extrusomes, 2.0–3.0 × 0.2–0.3 μm, are rod-shaped with tubular cores and identified as toxicysts, the aggregation of which in the anterior part of the theront and cortex of the trophont revealed their potential roles in I. multifiliis invasion. This was confirmed by our transcriptome investigations of the three stages of I. multifiliis, which revealed that a set of genes involved in proteolysis and DNA/protein biogenesis was highly expressed in the theront and trophont. Furthermore, to map the molecular mechanisms of extrusome release, we characterized 25 Rab family genes in I. multifiliis and determined their expression profiles across the life cycle, reflecting the distribution patterns of the two extrusomes. Collectively, our data revealed that a highly developed extrusome system could play a potential role in the virulence of I. multifiliis, which facilitates a better understanding of the parasite’s development.https://www.tandfonline.com/doi/10.1080/21505594.2023.2242622Ichthyophthirius multifiliismorphologenesisRNA-seqtranscriptomeexosome |
| spellingShingle | Hao Yang Zhe Wang Jieyin Xiao Jingbo Hu Xiao Tu Zemao Gu Integrated morphological and transcriptome profiles reveal a highly-developed extrusome system associated to virulence in the notorious fish parasite, Ichthyophthirius multifiliis Virulence Ichthyophthirius multifiliis morphologenesis RNA-seq transcriptome exosome |
| title | Integrated morphological and transcriptome profiles reveal a highly-developed extrusome system associated to virulence in the notorious fish parasite, Ichthyophthirius multifiliis |
| title_full | Integrated morphological and transcriptome profiles reveal a highly-developed extrusome system associated to virulence in the notorious fish parasite, Ichthyophthirius multifiliis |
| title_fullStr | Integrated morphological and transcriptome profiles reveal a highly-developed extrusome system associated to virulence in the notorious fish parasite, Ichthyophthirius multifiliis |
| title_full_unstemmed | Integrated morphological and transcriptome profiles reveal a highly-developed extrusome system associated to virulence in the notorious fish parasite, Ichthyophthirius multifiliis |
| title_short | Integrated morphological and transcriptome profiles reveal a highly-developed extrusome system associated to virulence in the notorious fish parasite, Ichthyophthirius multifiliis |
| title_sort | integrated morphological and transcriptome profiles reveal a highly developed extrusome system associated to virulence in the notorious fish parasite ichthyophthirius multifiliis |
| topic | Ichthyophthirius multifiliis morphologenesis RNA-seq transcriptome exosome |
| url | https://www.tandfonline.com/doi/10.1080/21505594.2023.2242622 |
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