Sex steroids and steroidogenesis-related genes in the sea cucumber, Holothuria scabra and their potential role in gonad maturation

• Published in: Scientific reports Vol. 11; no. 1; pp. 2194 - 16
• Main Authors: Thongbuakaew, Tipsuda, Suwansa-ard, Saowaros, Chaiyamoon, Arada, Cummins, Scott F., Sobhon, Prasert
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 26-01-2021; Nature Publishing Group; Nature Portfolio
• Subjects: 17β-Estradiol; 631/337/2019; 631/601/1737; Amino Acid Sequence; Androgens; Animals; Aquaculture; Base Sequence; Comparative analysis; Estradiol - pharmacology; Estrogens; Evolutionary conservation; Gene expression; Gene Expression Regulation, Developmental - drug effects; Gonads - drug effects; Gonads - growth & development; Gonads - metabolism; Holothuria scabra; Holothuroidea; Humanities and Social Sciences; Invertebrates; Liquid chromatography; Mass spectrometry; Mass spectroscopy; Maturation; Molecular Sequence Annotation; multidisciplinary; Organ Specificity - drug effects; Organ Specificity - genetics; Ovaries; Phylogeny; Population decline; Progesterone; Progesterone - pharmacology; Science; Science (multidisciplinary); Sea Cucumbers - drug effects; Sea Cucumbers - genetics; Sex; Sexual Maturation - drug effects; Sexual Maturation - genetics; Species; Steroid hormones; Steroidogenesis; Steroidogenic acute regulatory protein; Steroids; Steroids - biosynthesis; Steroids - metabolism; Testes; Testosterone; Time Factors; Tissue Distribution - drug effects; Transcriptomes; Vegetables; Vertebrates; Vitellogenin; Vitellogenins - genetics; Vitellogenins - metabolism
• ISSN: 2045-2322; 2045-2322
• DOI: 10.1038/s41598-021-81917-x

The sea cucumber
Holothuria scabra
is an economically valuable marine species which is distributed throughout the Asia–Pacific region. With the natural population declining due to over fishing, aquaculture of this species is deemed necessary. Hence, it is essential to understand the mechanisms regulating the reproduction in order to increase their populations. Sex steroids, including estrogens, androgens and progestogens, play an important role in reproduction in most vertebrates and several invertebrates. It has been proposed that sea cucumbers have the same sex steroids as vertebrates but the steroidogenic pathway in the sea cucumbers is still unclear. In this study, we demonstrated by using liquid chromatography-tandem mass spectrometry (LC–MS/MS) that sex steroids (estradiol, progesterone, and testosterone) were present in
H. scabra
neural and gonadal tissues
.
In silico searches of available sea cucumber transcriptome data identified 26 steroidogenesis-related genes. Comparative analysis of encoded proteins for the steroidogenic acute regulatory protein (HscStAR), CYP P450 10, 17 and 3A (HscCYP10, HscCYP17, HscCYP3A) and hydroxysteroid dehydrogenases (Hsc3β-HSD, Hsc17β-HSD) with other species was performed to confirm their evolutionary conservation. Gene expression analyses revealed widespread tissue expression. Real-time PCR analysis revealed that
HscStAR
,
HscCYP10
,
Hsc3β-HSD,
and
Hsc17β-HSD
gene expressions were similar to those in ovaries and testes, which increased during the gonad maturation.
HscCYP17
mRNA was increased during ovarian development and its expression declined at late stages in females but continued high level in males. The expression of the
HscCYP3A
was high at the early stages of ovarian development, but not at other later stages in ovaries, however it remained low in testes. Moreover, a role for steroids in reproduction was confirmed following the effect of sex steroids on vitellogenin (Vtg) expression in ovary explant culture, showing upregulation of Vtg level. Collectively, this study has confirmed the existence of steroids in an echinoderm, as well as characterizing key genes associated with the steroidogenic pathway. We propose that sex steroids might also be associated with the reproduction of
H. scabra
, and the identification of biosynthetic genes enables future functional studies to be performed.