The parasitic dinoflagellate Hematodinium spp. is an endoparasitic dinoflagellate infecting a wide range of marine decapod crustaceans. To date, it could infect more than 40 species of marine crustaceans, leading to Hematodinium epizootics and causing substantial economic losses to multiple commercially valuable marine crustaceans worldwide.

Hematodinium spp. mainly resides and proliferates in hosts' hemolymph or haemocoel, causing tissue damage and malfunction of infected organs eventually leading to hosts' mortality in late stages of infection. In decades, H. perezi has become an emerging infectious pathogen in the coastal waters of China.

Recently, the research team led by Prof. LI Caiwen from the Institute of Oceanology of the Chinese Academy of Sciences (IOCAS) provided comprehensive and novel insights into the immunomodulatory effects of H. perezi on crustacean host immunity.

The study was published in Fish and Shellfish Immunology on May. 5.

Researchers used the omics technology including miRNA transcriptomics and isobaric tags for relative and absolute quantification (iTRAQ)-based proteomics to systematically explore the host-parasite interaction between hemocytes from Portunus trituberculatus and H. perezi.

Hematodinium perezi significantly affected the miRNome and proteome profiles of hemocytes from challenged hosts, regulated the host immune response at post-transcriptional and translational levels and resulted in post-transcriptional regulation to the crustacean host immunity.

Multiple key immune-related pathways such as Apoptosis, Endocytosis, Extracellular matrix (ECM)-receptor interaction, prophenoloxidase (proPO) activation pathway, Toll-like signaling pathway, and Janus kinase (Jak)-Signal Transducers and Activators of Transcription (STAT) signaling pathway were influenced obviously by H. perezi.

By modulating the host miRNome, the host immune responses of nodulation, proPO activation and antimicrobial peptides were suppressed significantly. The host's cellular homeostasis was imbalanced with the phagosome and peroxisome pathways dysregulated post-transcriptionally. Cellular structure and communication was impacted severely via post-transcriptional downregulation of ECM-receptor interaction and focal adhesion pathways.

"The immune responses of crustaceans against viral and bacterial pathogens been extensively studied. However, the current knowledge on the interaction between parasites and their crustacean hosts is still extremely limited. This work provides fundamental knowledge on the host-parasite interaction of a parasitic dinoflagellate and its crustacean host, which will contribute to a greater understanding of crustacean immune response," said Dr. LI Meng, first author of the study.

"Studies on immunomodulatory effects of H. perezi on crustacean immunity will contribute to a better understanding of the molecular mechanism of the particular host-parasite interaction, as wells as the parasitic strategy of the parasitic dinoflagellate," said Prof. LI.

The research was supported by the NSFC-Shandong Joint-funding Program of National Natural Science Foundations of China, the China youth project of the National Natural Science Foundation of China, the Key Deployment Project of Centre for Ocean Mega-Science, Chinese Academy of Sciences, etc.

Expression analysis of the identified miRNAs and proteins in hemocytes (A), and hierarchical clustering of the 44 differentially expressed miRNAs (DEMs) in hemocytes post Hematodinium challenge (B), and the significantly enriched immune-related KEGG (Kyoto Encyclopedia of Genes and Genomes) pathways of the predicted target genes of DEMs (C).

Li, M., Huang, Q., Lv X.Y., Small, H.J., Li, C.W. (2022). Integrative omics analysis highlights the immunomodulatory effects of the parasitic dinoflagellate hematodinium on crustacean hemocytes. Fish and Shellfish Immunology, 125: 35-47.

LI Caiwen

Institute of Oceanology

E-mail: cwli@qdio.ac.cn

(Editor: ZHANG Yiyi)