Potential role of oocyte-intrinsic fatty acid synthesis in ovarian development of the bigfin reef squid Sepioteuthis lessoniana

Abstract

In most animals, excess dietary energy is stored as lipids in specialized tissues, such as the liver in vertebrates or the hepatopancreas and fat body in invertebrates, which function as energy reservoirs for reproduction. In cephalopods, however, dietary energy is rapidly mobilized from the digestive gland for growth rather than stored for reproduction. How excess energy is allocated for reproduction activity in cephalopods remains largely unclear. Lipogenesis is initiated by acetyl-CoA carboxylase (ACC), which converts acetyl-CoA derived from dietary carbon sources into malonyl-CoA; subsequent synthesis of saturated fatty acids is catalyzed by fatty acid synthase (FAS). Using the bigfin reef squid as a model, we investigate the role of fas in female development. fas mRNA was highly expressed in ovaries but weak in other tissues, including the lipid-rich digestive gland. fas showed female-biased expression in gonads, with level highest in juvenile ovaries and progressively decreasing to their lowest in mature ovaries. Expression was also high in primary and multiple follicular oocytes but declined in later stages. In situ hybridization and immunohistochemistry confirmed fas mRNA and protein localization in oocytes, particularly in primary and multiple follicular oocytes. In vitro ovarian culture further showed that inhibiting FAS activity enhanced somatic cell proliferation. Together, these findings suggest that squid ovary is a primary site of fatty acid synthesis, supporting early oocyte growth and membrane biogenesis in the absence of dedicated lipid storage tissues. The decline of FAS activity during oogenesis, and the associated reproduction in fatty acid synthesis, may act as a regulatory signal to promote somatic cell proliferation.