External immune sentinels in the seawater ecosystem: the specialization of bivalve hemocytes

Immune sentinel cells in vertebrates play key roles in coordinating immune responses at the organism-environment interface. We describe a system in marine bivalves that could be analogous, with immune sentinel hemocytes (ISCs) that function on the surface of the organism but which could be specialized to act also outside the body. In bivalves, hemocytes migrate into the intervalvar cavity and surrounding seawater, where they remain viable, exhibit an immune-activated transcriptomic profile and tolerate acute infections. The key novel findings of mussel ISCs include: i) transfer between individuals, ii) apoptosis resistance, and iii) lack of allorecognition. Their transcriptomic profiles partially overlap with transmissible neoplastic hemocytes, but they retain a distinct functional immune identity. The functional characterization and visualization of ISCs in the marine ecosystem uncovers their potential for transfer between individuals. The description of this externalized immune defense system might constitute an evolutionary adaptation in marine invertebrates, advancing the understanding of population-level immunity.