Molecular Approaches Detect Early Signals of Programmed Cell Death in Hippolyte inermis Leach

Author:

Glaviano Francesca1,Esposito Roberta2,Somma Emanuele13,Sagi Amir4,Aflalo Eliahu D.45ORCID,Costantini Maria2ORCID,Zupo Valerio1ORCID

Affiliation:

1. Department of Integrative Marine Ecology, Ischia Marine Centre, Stazione Zoologica Anton Dohrn, 80077 Ischia, Italy

2. Department of Ecosustainable Marine Biotechnology, Stazione Zoologica Anton Dohrn, Via Ammiraglio Ferdinando Acton n. 55, 80133 Naples, Italy

3. Department of Life Science, University of Trieste, Via L. Giorgieri, 10, 34127 Trieste, Italy

4. Department of Life Sciences, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva 8410501, Israel

5. Department of Life Sciences, Achva Academic College, Arugot 7980400, Israel

Abstract

The protandric shrimp Hippolyte inermis is the only known marine invertebrate whose sex determination is strongly influenced by the composition of its food. In H. inermis, a sex reversal is triggered by the ingestion of diatoms of the genus Cocconeis associated with leaves of the seagrass Posidonia oceanica. These diatoms contain compounds that promote programmed cell death (PCD) in H. inermis and also in human cancer cells. Transcriptomic analyses suggested that ferroptosis is the primary trigger of the shrimp’s sex reversal, leading to the rapid destruction of the androgen gland (AG) followed by a chain of apoptotic events transforming the testes into ovaries. Here, we propose a molecular approach to detect the effects of compounds stimulating the PCD. An RNA extraction method, suitable for young shrimp post-larvae (five days after metamorphosis; PL5 stage), was established. In addition, six genes involved in apoptosis, four involved in ferroptosis, and seven involved in the AG switch were mined from the transcriptome, and their expression levels were followed using real-time qPCR in PL5 fed on Cocconeis spp., compared to PL5 fed on a basic control feed. Our molecular approach, which detected early signals of sex reversal, represents a powerful instrument for investigating physiological progression and patterns of PCD in marine invertebrates. It exemplifies the physiological changes that may start a few days after the settlement of post-larvae and determine the life destiny of an individual.

Funder

Italian Ministry for Foreign Affairs, Grant Excites

Israel Ministry of Science and Technology, Grant Excites

CRIMAC

Publisher

MDPI AG

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4. Ankeny, R., and Leonelli, S. (2020). Model Organisms, Cambridge University Press. [3rd ed.].

5. Evolution of sex determination in crustaceans;Ye;Mar. Life Sci. Technol.,2023

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