Morpho-functional characterisation of cœlomocytes in the aquacultivated sea cucumber Holothuria scabra: From cell diversity to transcriptomic immune response

Holothuria scabra is one of the most valuable species of sea cucumber owing to its exploitation as a seafood product. This study aims to describe the main molecular and cellular actors in the immunology of this species. First, a detailed description of the immune cells - the cœlomocytes - is provided, highlighting five main cell types including phagocytes, small round cells (SRCs), spherulocytes, fusiform cells, and crystal cells, with a further five subtypes identified using transmission electron microscopy. Cœlomocyte aggregates were also described morphologically, yielding two main types, one comprising three successive maturation stages. A comparison of the concentration and proportion of cell populations was carried out between the two main body fluids, namely the hydrovascular fluid of the Polian vesicle (HF) and the perivisceral fluid of the general cavity (PF), and no clear relation could be highlighted. Next, the cœlomocyte immune response was studied 24 h after lipopolysaccharide (LPS) injection in the two body fluids. Firstly, the fluctuation in cell populations was assessed, and despite a high inter-individual variability, it shows a decrease in the phagocyte proportion and an increase in the SRC proportion. Secondly, the differential gene expression of PF cœlomocytes was studied by de novo RNA-sequencing between LPS-injected and control-injected individuals: 945 genes were differentially expressed, including 673 up-regulated and 272 down-regulated in the LPS-injected individuals. Among these genes, 80 had a presumed function in immunity based on their annotation, covering a wide range of immune mechanisms. Overall, this study reveals a complex immune system at both molecular and cellular levels and constitutes a baseline reference on H. scabra immunity, which may be useful for the development of sustainable aquaculture and provides valuable data for comparative immunology.