Highly Sensitive and Specific Responses of Oyster Hemocytes to Copper Exposure: Single-Cell Transcriptomic Analysis of Different Cell Populations

Oyster hemocytes are the primary
vehicles transporting and detoxifying
metals and are regarded as important cells for the occurrence of colored
oysters due to copper (Cu) contamination. However, its heterogeneous
responses under Cu exposure have not been studied. Single-cell transcriptome
profiling (scRNA-seq) provides high-resolution visual insights into
tissue dynamics and environmental responses. Here, we used scRNA-seq
to study the responses of different cell populations of hemocytes
under Cu exposure in an estuarine oyster Crassostrea
hongkongensis. The 1900 population-specific Cu-responsive
genes were identified in 12 clusters of hemocytes, which provided
a more sensitive technique for examining Cu exposure. The granulocyte,
semigranulocyte, and hyalinocyte had specific responses, while the
granulocyte was the most important responsive cell type and displayed
heterogeneity responses of its two subtypes. In one subtype, Cu was
transported with metal transporters and chelated with Cu chaperons
in the cytoplasm. Excess Cu disturbed oxidative phosphorylation and
induced reactive oxygen species production. However, in the other
subtype, endocytosis was mainly responsible for Cu internalization,
which was sequestered in membrane-bound granules. Collectively, our
results provided the first mRNA expression profile of hemocytes in
oysters and revealed the heterogeneity responses under Cu exposure.