CAS Key Lab of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China; Marine Ecology and Environmental Science Laboratory, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China; Centre for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, 266071, China.
CAS Key Lab of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China; University of Chinese Academy of Sciences, Beijing, 100049, China.
Fish Shellfish Immunol. 2022 Jun;125:35-47. doi: 10.1016/j.fsi.2022.04.050. Epub 2022 May 5.
Parasitic dinoflagellates in genus Hematodinium have caused substantial economic losses to multiple commercially valuable marine crustaceans around the world. Recent efforts to better understand the life cycle and biology of the parasite have improved our understanding of the disease ecology. However, studies on the host-parasite interaction, especially how Hematodinium parasites evade the host immune response are lacking. To address this shortfall, we used the comprehensive omics approaches (miRNA transcriptomics, iTRAQ-based proteomics) to get insights into the host-parasite interaction between hemocytes from Portunus trituberculatus and Hematodinium perezi in the present study. The parasitic dinoflagellate H. perezi remodeled the miRNome and proteome of hemocytes from challenged hosts, modulated the host immune response at both post-transcriptional and translational levels and caused post-transcriptional regulation to the host immune response. Multiple important cellular and humoral immune-related pathways (ex. Apoptosis, Endocytosis, ECM-receptor interaction, proPO activation pathway, Toll-like signaling pathway, Jak-STAT signaling pathway) were significantly affected by Hematodinium parasites. Through modulation of the host miRNome, the host immune responses of nodulation, proPO activation and antimicrobial peptides were significantly suppressed. Cellular homeostasis was imbalanced via post-transcriptional dysregulation of the phagosome and peroxisome pathways. Cellular structure and communication was seriously impacted by post-transcriptional downregulation of ECM-receptor interaction and focal adhesion pathways. In conclusion, H. perezi parasites could trigger striking changes in the miRNome and proteome of crustacean hemocytes, and this parasite exhibited multifaceted immunomodulatory effects and potential immune-suppressive mechanisms in crustacean hosts.
寄生性甲藻属中的 Hematodinium 已经对全球多种具有商业价值的海洋甲壳类动物造成了巨大的经济损失。最近，人们为了更好地了解寄生虫的生命周期和生物学特性，已经对寄生虫的疾病生态学有了更深入的了解。然而，有关宿主-寄生虫相互作用的研究，尤其是 Hematodinium 寄生虫如何逃避宿主免疫反应的研究还很缺乏。为了解决这一不足，我们在本研究中使用了全面的组学方法（miRNA 转录组学、iTRAQ 蛋白质组学）来深入了解三疣梭子蟹血细胞与 Hematodinium perezi 之间的宿主-寄生虫相互作用。寄生性甲藻 H. perezi 重塑了受感染宿主血细胞的 miRNome 和 proteome，在转录后和翻译水平上调节了宿主的免疫反应，并导致宿主免疫反应的转录后调控。多个重要的细胞和体液免疫相关途径（如凋亡、内吞作用、细胞外基质-受体相互作用、原酚氧化酶激活途径、Toll 样信号通路、Jak-STAT 信号通路）受到 Hematodinium 寄生虫的显著影响。通过宿主 miRNome 的调节，宿主的结节、原酚氧化酶激活和抗菌肽的免疫反应受到显著抑制。通过对吞噬体和过氧化物酶体途径的转录后失调，细胞内稳态失衡。通过对细胞外基质-受体相互作用和焦点黏附途径的转录后下调，细胞结构和通讯受到严重影响。总之，H. perezi 寄生虫可以引发甲壳类动物血细胞的 miRNome 和 proteome 发生显著变化，并且这种寄生虫在甲壳类动物宿主中表现出多方面的免疫调节作用和潜在的免疫抑制机制。
