Changes in Menidia beryllina Gene Expression and In Vitro Hormone-Receptor Activation After Exposure to Estuarine Waters Near Treated Wastewater Outfalls

Abstract

Fishes in estuarine waters are frequently exposed to treated wastewater effluent, among numerous other sources of contaminants, yet the impacts of these anthropogenic chemicals are not well understood in these dynamic and important waterways. Inland silversides (Menidia beryllina) at an early stage of development [12 days posthatch (dph)] were exposed to waters from two estuarine wastewater-treatment outfall locations in a tidal estuary, the Sacramento/San Joaquin Delta (California, USA) that had varied hydrology and input volumes. The genomic response caused by endocrine-disrupting compounds (EDCs) in these waters was determined using quantitative polymerase chain reaction on a suite of hormonally regulated genes. Relative androgenic and estrogenic activities of the waters were measured using CALUX reporter bioassays. The presence of bifenthrin, a pyrethroid pesticide and known EDC, as well as caffeine and the anti-inflammatory pharmaceutical ibuprofen, which were used as markers of wastewater effluent input, were determined using instrumental analysis. Detectable levels of bifenthrin (2.89 ng L(-1)) were found on one of the sampling dates, and caffeine was found on all sampling dates, in water from the Boynton Slough. Neither compound was detected at the Carquinez Strait site, which has a much smaller effluent discharge input volume relative to the receiving water body size compared with Boynton Slough. Water samples from both sites incubated in the CALUX cell line induced estrogenic and androgenic activity in almost all instances, though the estrogenicity was relatively higher than the androgenicity. Changes in the abundance of mRNA transcripts of endocrine-responsive genes and indicators of general chemical stress were observed after a 96-h exposure to waters from both locations. The relative levels of endocrine response, changes in gene transcript abundance, and contaminant concentrations were greater in water from the Boynton Slough site despite those effluents undergoing a more advanced treatment process. The availability of a widely geographically distributed estuarine model species (M. beryllina) now allows for improved assessment of treated effluent impacts across brackish, estuarine, and marine environments.

Impacts of Salinity and Temperature on the Thyroidogenic Effects of the Biocide Diuron in Menidia beryllina

“…Water samples collected in the Sacramento–San Joaquin Delta altered the expression at the mRNA level of endocrine responsive genes such as gonadal aromatase (CYP19a), androgen, estrogen, and thyroid receptors . Endocrine active materials in water were also observed from similar locations in the Central Valley and San Francisco Bay Delta .…”

Early Life Exposure to Environmentally Relevant Levels of Endocrine Disruptors Drive Multigenerational and Transgenerational Epigenetic Changes in a Fish Model

“…Endocrine disrupting chemicals (EDCs) include a variety of compound classes such as pesticides, pharmaceuticals, industrial chemicals, and metals, that are grouped together on the basis of their tendency to alter hormone signaling. Many EDCs enter the aquatic environment through runoff and wastewater, allowing them to move into estuarine and marine systems (Ribeiro et al, 2009;Bayen et al, 2013;Brander, 2013;Cole et al, 2016;DeCourten et al, 2019b;Zhou et al, 2019). Even at low levels (ng/L), EDC exposure during early development has been implicated in causing a variety of effects in fish across biological scales, including changes in growth and development, reproduction, immune function, sex ratio, gene expression, and DNA methylation (Hinck et al, 2008;Schug et al, 2016).…”

“…Even at low levels (ng/L), EDC exposure during early development has been implicated in causing a variety of effects in fish across biological scales, including changes in growth and development, reproduction, immune function, sex ratio, gene expression, and DNA methylation (Hinck et al, 2008;Schug et al, 2016). For example, a growing body of literature has linked molecular endpoints to physiological and behavioral endpoints of EDC exposure in the ecologically and toxicologically relevant inland silverside, Menidia beryllina, an estuarine species common in North America (Brander et al, 2016;Cole et al, 2016;DeCourten and Brander, 2017;DeCourten et al, 2019b;Frank et al, 2019). Multi-and transgenerational effects of EDC exposure have been documented in M. beryllina, sometimes with latent effects occurring in the F1 generation (indirectly exposed as primordial germ cells), reinforcing concern for longterm population-level impacts from these ubiquitous environmental chemicals (DeCourten and Brander, 2017;DeCourten et al, 2019a;DeCourten et al, unpublished).…”

Review of and Recommendations for Monitoring Contaminants and their Effects in the San Francisco Bay−Delta

“…The sequenced genome provides information needed to evaluate responses at the epigenomic level. Transcriptomic and proteomic scale data also exists for this species (Brander et al 2016a;Cole et al 2016), and behavioral assays comparable to those used for Zebrafish have recently been validated (Frank et al 2019). This allows for the development of high-throughput assays that evaluate a diversity of responses, which can be used in a species of concern to rapidly provide answers to a wide range of questions.…”