Transcriptomic profiles of Florida pompano (Trachinotus carolinus) gill following infection by the ectoparasite Amyloodinium ocellatum

Authors: ZHANG, DONGDONG - Auburn University; MOHAMMED, HAITHAM - Auburn University; YE, ZHI - Auburn University; RHODES, MELANIE - Auburn University; THONGDA, WILAWAN - Auburn University; ZHAO, HONGGANG - Auburn University; JESCOVITCH, LAUREN - Auburn University; Fuller, Adam; DAVIS, A. ALLEN - Auburn University; PEATMAN, ERIC - Auburn University

Submitted to: Fish and Shellfish Immunology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/12/2022
Publication Date: 5/13/2022
Citation: Zhang, D., Mohammed, H., Ye, Z., Rhodes, M., Thongda, W., Zhao, H., Jescovitch, L., Fuller, S.A., Davis, A., Peatman, E. 2022. Transcriptomic profiles of Florida pompano (Trachinotus carolinus) gill following infection by the ectoparasite Amyloodinium ocellatum. Fish and Shellfish Immunology. 125:171-179. https://doi.org/10.1016/j.fsi.2022.05.017.
DOI: https://doi.org/10.1016/j.fsi.2022.05.017

Interpretive Summary: Amyloodinium ocellatum is an important disease-causing parasite infecting cultured marine and brackish water fishes worldwide. This includes cultured Florida pompano, which is one of the most desirable marine food fish with high economic value in the USA. This parasite infects fish gills and causes tissue damage, increased respiratory rate, reduced appetite, and mortality, especially in closed aquaculture systems. This study mimicked the natural infection of A. ocellatum in cultured pompano and conducted a study to determine which genes from the fish’s DNA were converted to make specific proteins, a term called gene expression, following exposure to a A. ocellatum infection. RNA-sequencing data revealed 604 differentially expressed genes in the infected fish gills. Genes involved with immune response and inflammation suppression were detected after infection. Genes involved in reactive oxygen species (ROS) mediating parasite killing were also highly activated. However, too many ROSs have been linked to oxidative tissue damage and cell death (apoptosis). Also, widespread down-regulation of collagen genes and lack of growth factors indicated impaired tissue repair, while the main gene involved in cell death was highly expressed in parasite-infected fish. The infection also affected the respiratory gas sensing and transport genes and established low oxygen, or hypoxic conditions in the gill tissue. Additionally, food intake and fat metabolism were also affected. Our work provides the first gene expression sequencing of Florida pompano and provides key insights into the how this parasitic disease affects pompano shortly after infection. This information can be utilized for designing optimal disease monitoring strategies, future selection for pompano parasitic resistance, and development of new drug treatments measures.

Technical Abstract: The dinoflagellate Amyloodinium ocellatum is an important pathogenic parasite infecting cultured marine and brackish water fishes worldwide. This includes cultured Florida pompano (Trachinotus carolinus), which is one of the most desirable marine food fish with high economic value in the USA. A. ocellatum infects fish gills and causes tissue damage, increased respiratory rate, reduced appetite, and mortality, especially in closed aquaculture systems. This study mimicked the natural infection of A. ocellatum in cultured pompano and conducted a transcriptomic comparison of gene expression in the gills of control and A. ocellatum infected fish to explore the molecular mechanisms of infection. RNA-seq data revealed 604 differentially expressed genes in the infected fish gills. The immunoglobulin genes (including IgM/T), augmentation and IL1 inflammation suppression were detected after infection. Genes involved in reactive oxygen species mediating parasite killing were also highly induced. However, excessive oxidants have been linked to oxidative tissue damage and apoptosis. Correspondingly, widespread down-regulation of collagen genes and growth factor deprivation indicated impaired tissue repair, while the key executor of apoptosis, caspase-3 was highly expressed (25.02-fold) in infected fish. The infection also influenced the respiratory gas sensing and transport genes and established hypoxic conditions in the gill tissue. Additionally, food intake and lipid metabolism were also affected. Our work provides the first transcriptome sequencing of Florida pompano and provides key insights into the acute pathogenesis of A. ocellatum. This information can be utilized for designing optimal disease surveillance strategies, future selection for host resistance, and development of novel therapeutic measures.