Effects of bisphenol A on the development of pigmented organs in the ascidian Phallusia mammillata

Abstract

Bisphenol A (BPA) is an organic compound that is used in the manufacture of polycarbonate plastic and epoxy resins and is increasingly being released into the environment. BPA can act as a teratogenic substance and an endocrine disruptor, raising concerns about its impact on humans and wildlife. Thus, in the present work, we evaluated the effects of different concentrations of BPA on ontogenetic processes in the ascidian Phallusia mammillata. The phylogenetic position of ascidians, their cosmopolitan distribution in marine ecosystems, and multiple technical advantages associated with their biology make ascidians reliable model organisms for ecotoxicology bioassays. Our investigations showed that BPA did not affect the capability of ascidian sperm to fertilize eggs, but it impaired embryonic development and caused a phenotype that was characterized by a short and kinked tail. Larvae developed from BPA-exposed embryos also presented malformations of pigmented organs such as altered pigment deposition, absence of one or both pigmented organs, and supernumerary organs. The co-exposure with 4-hydroxytamoxifen, an estrogen-related receptor (ERR) inverse agonist, rescued the normal phenotype of pigmented organs, thus supporting the hypothesis that, in ascidians, BPA exerts its teratogenic effects mainly by binding to ERR, as in vertebrate models. K E Y W O R D Snervous system, ocellus, otolith, rescue of function, tunicate

Potential roles of nuclear receptors in mediating neurodevelopmental toxicity of known endocrine‐disrupting chemicals in ascidian embryos

“…At sublethal doses, BPA has been shown to delay larval development in copepods and molluscs, to induce changes in immune digestive gland function in marine bivalves, or to stimulate metamorphosis and larval development in marine polychaetes and copepods (Canesi & Fabbri, ), with effective concentrations ranging from 0.01 up to 300 µg/µl (Flint et al, ). Furthermore, BPA and other known vertebrate EDCs, such as diuron and diethylstilbestrol specifically affect neurodevelopment in ascidians at low doses, as recently reported (Dumollard, Gazo, Gomes, Besnardeau, & McDougall, ; Messinetti, Mercurio, & Pennati, ; Messinetti, Mercurio, & Pennati, ). However, apart from the phenotypes and dose‐response sensitivity, few studies assessed the mode‐of‐action and even fewer addressed the potential involvement of NRs in the teratogenic effects of EDCs in marine invertebrates.…”

“…As previously reported, BPA and other EDCs induce neurodevelopmental toxicity in ascidians (Dumollard et al, ; Matsushima, Ryan, Shimohigashi, & Meinertzhagen, ; Messinetti et al, , ). The CNS of the ascidian larvae is divided into three parts: An anterior brain sensory vesicle, a trunk ganglion, and a caudal nerve cord (Figure ; Hudson, ).…”

“…In our laboratory, we have discovered recently that BPA (and other bisphenols) consistently reduced pigmentation and inhibited the movement of the Ot cell within the sensory vesicle of Phallusia mammillata larvae whereas other neural structures, such as the palps are not affected (Gomes et al, in preparation). The GRN driving specification of the pigmented cells does not seem to be affected (Messinetti et al, , Gomes et al, in preparation) suggesting that the differentiation of pigmented cells is more likely affected by EDCs.…”

Embryotoxicity characterization of the flame retardant tris(1‐chloro‐2‐propyl)phosphate (TCPP) in the invertebrate chordate Ciona intestinalis

“…These organisms are important members of the marine benthic community, contributing to increase ecosystem biodiversity through the colonization of different natural and artificial substrates (Sepúlveda et al, 2014). In the last few years, ascidians have been recognized as reliable model systems for ecotoxicological research, thanks to their wide distribution and ecology as well as for their rapid embryonic development, and high production of gametes (Eliso et al, 2020; Messinetti et al, 2018; Messinetti, Mercurio, & Pennati, 2019). In particular, we employed Ciona intestinalis as a model organism and focused on TCPP's adverse effects on embryonic development, that is, one of the most sensitive stages of animal lifecycle.…”

Fluorescence Properties of a Novel Isoquinoline Derivative Tested in an Invertebrate Chordate, Ciona intestinalis

“…Ascidians are marine organisms closely related to vertebrates [6,7] . They have been successfully used to assess the effects of several chemicals on animal development and behaviour [8,9] . Adults are sessile filter‐feeding animals that develop through a free‐swimming larva.…”