Multinucleated giant hemocytes (MGHs) represent a novel type of blood cell in insects
that participate in a highly efficient immune response against parasitoid wasps involving
isolation and killing of the parasite. Previously, we showed that circulating MGHs
have high motility and the interaction with the parasitoid rapidly triggers encapsulation.
However, structural and molecular mechanisms behind these processes remained elusive.
Here, we used detailed ultrastructural analysis and live cell imaging of MGHs to study
encapsulation in Drosophila ananassae after parasitoid wasp infection. We found
dynamic structural changes, mainly driven by the formation of diverse vesicular systems
and newly developed complex intracytoplasmic membrane structures, and abundant generation
of giant cell exosomes in MGHs. In addition, we used RNA sequencing to study the transcriptomic
profile of MGHs and activated plasmatocytes 72 h after infection, as well as the uninduced
blood cells. This revealed that differentiation of MGHs was accompanied by broad changes
in gene expression. Consistent with the observed structural changes, transcripts related
to vesicular function, cytoskeletal organization, and adhesion were enriched in MGHs.
In addition, several orphan genes encoding for hemolysin-like proteins, pore-forming
toxins of prokaryotic origin, were expressed at high level, which may be important
for parasitoid elimination. Our results reveal coordinated molecular and structural
changes in the course of MGH differentiation and parasitoid encapsulation, providing
a mechanistic model for a powerful innate immune response.
