Mugilid Fish Are Sentinels of Exposure to Endocrine Disrupting Compounds in Coastal and Estuarine Environments

Abstract

Effects on fish reproduction can result from a variety of toxicity mechanisms first operating at the molecular level. Notably, the presence in the environment of some compounds termed endocrine disrupting chemicals (EDCs) can cause adverse effects on reproduction by interfering with the endocrine system. In some cases, exposure to EDCs leads to the animal feminization and male fish may develop oocytes in testis (intersex condition). Mugilid fish are well suited sentinel organisms to study the effects of reproductive EDCs in the monitoring of estuarine/marine environments. Up-regulation of aromatases and vitellogenins in males and juveniles and the presence of intersex individuals have been described in a wide array of mullet species worldwide. There is a need to develop new molecular markers to identify early feminization responses and intersex condition in fish populations, studying mechanisms that regulate gonad differentiation under exposure to xenoestrogens. Interestingly, an electrophoresis of gonad RNA, shows a strong expression of 5S rRNA in oocytes, indicating the potential of 5S rRNA and its regulating proteins to become useful molecular makers of oocyte presence in testis. Therefore, the use of these oocyte markers to sex and identify intersex mullets could constitute powerful molecular biomarkers to assess xenoestrogenicity in field conditions.

Alteration in molecular markers of oocyte development and intersex condition in mullets impacted by wastewater treatment plant effluents

“…Only two intersex individuals could be studied at Galindo, and the one identified in February showed levels in between ovaries and normal testes. gtf3a codes for the transcription factor necessary for RNA polymerase III driven synthesis of 5S rRNA, that is accumulated in oocytes to assist quick ribosome assembly for protein production during early embryogenesis (Diaz de Cerio et al, 2012;Ortiz-Zarragoitia et al, 2014;Rojo-Bartolomé et al, 2016). Consequently, transcription of 5S rRNA and gtf3a mark the presence of oocytes , also when they are produced within the testis.…”

“…This alteration has been described in different wild fish species belonging to a wide range of families (Bahamonde et al, 2013;Jobling and Tyler, 2003;Ortiz-Zarragoitia et al 2014). Intersex fish show transcription patterns of oocyte development related genes resembling those in normal ovaries (Bahamonde et al, 2013;Diaz de Cerio et al, 2012).…”

“…The 5S rRNA molecule is necessary for the oocyte development and maturation process, due to its role in the production of ribosomes. Its accumulation during oocyte growth is crucial for the successful development of the fertilized egg, as this will enable to expedite protein synthesis during early embryo development (Lubzens et al, 2010;Diaz de Cerio et al, 2012;Mazabraud et al, 1975;Ortiz-Zarragoitia et al, 2014).…”

“…In the Basque coastal region, thicklip grey mullets have been used as sentinel organisms of endocrine disruption Diaz de Cerio et al, 2012;Ortiz-Zarragoitia et al, 2014;Puy-Azurmendi et al, 2013). Xenoestrogenic effects on mullets, such as up-regulation of vitellogenin and cyp19a1b transcription levels, have been related to elevated concentrations of some EDCs such as alkylphenols, pesticides, phthalates, musk fragrances, bisphenol A and oestrogenic hormones in the bile Puy-Azurmendi et al, 2013).…”

Effects of insecticides on aquatic ecosystems in Bangladesh

“…The intersex condition of fish indicates a low reproduction capacity and is a threat for fecundity as well as for population viability (Harris et al, 2011). The intersexuality in this study is probably due to the xenoestrogens released from endocrine-disrupting chemicals (EDCs), such as chlorpyrifos, altering normal sexual differentiation and gametogenesis because they interfere with synthesis, storage, release, transport, metabolism, binding action and elimination of endogenous hormones (Mills and Chichester, 2005;Ortiz-Zarragoitia, 2014). Xenoestrogens are structurally similar to 17β -estradiol (E2), such as 17α -ethinylestradiol (EE2), which exert their estrogenic effects on gonadal differentiation by mimicking the actions of endogenous estrogens and thereby inducing phenotypic feminization (Andersen et al, 2003;Kuhl et al, 2005).…”