Potential trade-offs between biomineralization and immunity revealed by shell properties and gene expression profiles of two closely related Crassostrea species

Abstract

Species of Ostreidae family are key ecosystem engineers and many of them (including Crassostrea gigas and C. virginica) are commercially important aquaculture species. Despite similarities in their morphology and ecology, these two species differ in their ability to defend against pathogens potentially reflecting species-specific differential specialization of hemocytes on immune defense vs. biomineralization. To test this hypothesis, we investigated the expression levels of immune and biomineralization-related genes as well as mineralogical and mechanical properties of the shells and the calcium sequestration ability of the hemocytes of C. gigas and C. virginica. The expression of biomineralization related genes was higher in C. virginica than in C. gigas in multiple tissues including mantle edge and hemocytes, while the expression of immune genes was higher in the hemocytes of C. gigas. Hemocytes of C. virginica contained more calcium (stored intracellularly as calcium carbonate mineral) compared with those of C. gigas. Analysis of the adult shells showed that the crystallinity of calcite was higher and the laths of the foliated layer of the shell were thicker in C. virginica than in C. gigas. Mechanically the shells of C. virginica were stiffer, harder and stronger than those of C. gigas. Taken together, our results show that the species-specific differences in physiology (such as disease resistance and exoskeleton properties) are reflected at the cellular and molecular levels in differential specialization of hemocytes on potentially competing functions (immunity and biomineralization) as well as different expression profiles of other tissues involved in biomineralization (such as the mantle edge).