Transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus

Abstract

Anthropogenic endocrine disruptors now contaminate all environments globally, with concomitant deleterious effects across diverse taxa. While most studies on endocrine disruption (ED) have focused on vertebrates, the superimposition of male sexual characteristics in the female dogwhelk, Nucella lapillus (imposex), caused by organotins, provides one of the most clearcut ecological examples of anthropogenically induced ED in aquatic ecosystems. To identify the underpinning mechanisms of imposex for this 'nonmodel' species, we combined Roche 454 pyrosequencing with custom oligoarray fabrication inexpensively to both generate gene models and identify those responding to chronic tributyltin (TBT) treatment. The results supported the involvement of steroid, neuroendocrine peptide hormone dysfunction and retinoid mechanisms, but suggested additionally the involvement of putative peroxisome proliferator-activated receptor (PPAR) pathways. Application of rosiglitazone, a well-known vertebrate PPARγ ligand, to dogwhelks induced imposex in the absence of TBT. Thus, while TBT-induced imposex is linked to the induction of many genes and has a complex phenotype, it is likely also to be driven by PPAR-responsive pathways, hitherto not described in invertebrates. Our findings provide further evidence for a common signalling pathway between invertebrate and vertebrate species that has previously been overlooked in the study of endocrine disruption.

The nuclear receptor gene family in the Pacific oyster, Crassostrea gigas, contains a novel subfamily group

“…In gastropods, exposure to TBT causes irreversible superimposition of male genital on females, a condition termed imposex, whilst in bivalve species, exposure to TBT causes growth reduction [30–32], and shell thickening [33–36]. The mechanism by which TBT affects mollusc species remains unclear, although hypotheses have been raised related to binding to and disruption of a putative molluscan RXR or RXR/peroxisome proliferator-activated receptor (PPAR) heterodimer [29, 37–47]. …”

Widespread contamination of coastal sediments in the Transmanche Channel with anti-androgenic compounds

“…Chemical contaminants with estrogen receptor agonist or androgen receptor antagonist activity are present in wastewater effluents (Hill et al, 2010;Sumpter and Jobling, 2013) and studies to date have indicated that the steroidal estrogens and possibly anti-androgens present in the receiving waters are causing the high levels of feminized fish present in some UK river sites (Jobling et al, 2006(Jobling et al, , 2009. Other EDCs such as organotins, which in the past were used in marine antifouling paints, have caused widespread masculinization of female gastropods and may act as ligands for different nuclear receptors involved in sexual differentiation rather than those for sex steroids (Pascoal et al, 2013;Titley-O'Neal et al, 2011).…”

Defining the role of omics in assessing ecosystem health: Perspectives from the Canadian environmental monitoring program

“…Assessing transcriptome responses in laboratory-reared animals exposed to water or sediment obtained from the field is an increasingly common method used in environmental assessments [4,[28][29][30][31][32]. Although sediment brought into the laboratory more accurately reflects the complex mixtures present in situ, it should not be considered field-based, and these studies are not further considered in the present review.…”