Divergent functions between perivisceral and hydrovascular fluids under immunological stress in sea cucumbers (Holothuria forskali)

Echinoderms have two main coelomic cavities in their body plan: the general perivisceral cavity containing the different organs and the hydrovascular cavity constituting a unique vascular system also known as the water vascular system. These two cavities are filled with a fluid whose composition is close to that of seawater, but which contains a large amount of metabolites and cells. These cells are called coelomocytes and constitute the main actor of echinoderm immunity. Different cell types have been described based on morphological criteria; it appears that sea cucumbers show the greatest diversity among the five classes of echinoderms at six to seven different types. While the immune response of perivisceral coelomocytes has already been studied in different species, the immune response of hydrovascular coelomocytes remains understudied and the differences in their immune response have not been investigated yet. In the present study, we investigated the transcriptomic response of coelomocytes to injections of lipopolysaccharide (LPS) – a molecule that mimics a bacterial infection – in the sea cucumber Holothuria forskali. Coelomocytes from both fluids were studied distinctly to compare their immune response. In addition, we attempted to correlate gene expression with the proportion of different coelomocyte types in each fluid by counting the cells (Fig. 1). Our results revealed 17,646 differentially expressed genes (DEGs) between control and LPS-injected individuals (by considering both fluids) and 5524 and 6420 DEGS specific to the perivisceral and hydrovascular fluid, respectively. Regarding the comparison of the two fluids, 2853 genes were DEGs when considering all individuals (i.e., control and LPS-injected individuals). Interestingly, the same analysis resulted in only 179 DEGs in control individuals but in 2773 DEGs in stressed individuals. These results suggest that in immunoquiescent conditions, the coelomocytes from both fluids have a similar function but that this function tends to change following the immunological stress. Furthermore, this change coincides with an increase in the concentration of hemocytes as a result of immunological stress that occurs only in the hydrovascular fluid. Finally, the functional annotation of DEGs offers precious information about the specific functions of coelomocytes in both fluids. This research raises interesting questions about the function of the hydrovascular system and coelomocytes and provides valuable data for comparative immunology.