Interplay between immune cell damage and depletion, population size, ecological factors and Picornavirus infection in the Venice Lagoon (Italy)

We monitored the mortality of the fan mussel Pinna nobilis (L.) in the Venice lagoon (North of Italy) during a period of one and half year (2023–2024) in two areas named Ottagono Alberoni (OA) and Coffa Val Grande (CV) reporting the disease condition for the period time 2024. Host and environmental factors (e.g. pen shell state of infection, size, immune cell depletion with activation of caspase-3, oxygen, temperature, salinity) were investigated and shown to influence morbidity and mortality progressiveness in the two areas. During the study period, Pinna nobilis Picornavirus ( PnPV ) caused systemic hemic infections in all examined individuals (100%) compromising the organelle compartment of the cells activating cell death. Ultrastructure revealed widespread viral replication organelles (vROs) occupying most of the host immune cells that arose from a total rearrangement of cell cytoskeleton that were dedicated to the virus machinery. Our results show a positive correlation between mortality rates and host size, with higher mortality affecting bigger/older individuals, although with local differences. CV pen shell population was characterized by smaller/younger individuals affected by milder viral infections and suffering lower mortality rates. Conversely, OA population presented larger individuals (adults) of P. nobilis affected by heavy viral infections that suffering a 100% mortality rate, leading to the extinction of that population by October 2024. Total Hemocyte Count (THC) was lower in OA (1.77 × 10 4 ±0.16 cell/ml) compared to CV (1.65 × 10 5 ±0.8 cells/ml) showing a negative correlation with viral load, connected with percentage of dead cells percentage, in turn correlated with animal size, suggesting that number of immune cells is regulated by the level of infection, and also age. Collection of hemolymph from the adductor muscle is safe practice for P. nobilis and should be explored to the evaluation of PnPV presence in the fan mussel residual population in the Mediterranean Sea.