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Adverse metabolic effects in fish exposed to contaminants of emerging concern in the field and laboratory.

ABSTRACT: Several metabolic parameters were assessed in juvenile Chinook salmon (Oncorhynchus tshawytscha) and staghorn sculpin (Leptocottus armatus) residing in two estuaries receiving wastewater treatment effluent and one reference estuary. We also conducted a laboratory study with fish dosed for 32 days with 16 of the most common contaminants of emerging concern (CECs) detected in feral fish. Several blood chemistry parameters and other indicators of health were measured in fish from the field and laboratory study that were used to assess potential metabolic disruption. The blood chemistry values observed in feral juvenile Chinook salmon were relatively consistent among fish collected from effluent-impacted sites and substantially different compared to reference site fish. These responses were more pronounced in Chinook salmon, which is supported by the disparity in accumulated CECs. The blood chemistry results for juvenile Chinook salmon collected at effluent-impacted sites exhibited a pattern generally consistent with starvation because of similarities to observations from studies of food-deprived fish; however, this response is not consistent with physical starvation but may be contaminant induced. The altered blood chemistry parameters are useful as an early indicator of metabolic stress, even though organismal characteristics (lipid content and condition factor) were not different among sites indicating an early response. Evidence of metabolic disruption was also observed in juvenile Chinook salmon that were exposed in the laboratory to a limited mixture of CECs; however, the plasma parameters were qualitatively different possibly due to exposure route, season, or the suite of CECs. Growth was impaired in the high-dose fish during the dosing phase and the low- and medium-dose fish assayed after 2 weeks of depuration. Overall, these results are consistent with metabolic disruption for fish exposed to CECs, which may result in early mortality or an impaired ability to compete for limited resources.

SUBMITTER: Meador JP

PROVIDER: S-EPMC5858870 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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Adverse metabolic effects in fish exposed to contaminants of emerging concern in the field and laboratory.

Meador James P JP Yeh Andrew A Gallagher Evan P EP

Environmental pollution (Barking, Essex : 1987) 20180501

Several metabolic parameters were assessed in juvenile Chinook salmon (Oncorhynchus tshawytscha) and staghorn sculpin (Leptocottus armatus) residing in two estuaries receiving wastewater treatment effluent and one reference estuary. We also conducted a laboratory study with fish dosed for 32 days with 16 of the most common contaminants of emerging concern (CECs) detected in feral fish. Several blood chemistry parameters and other indicators of health were measured in fish from the field and labo ...[more]

PMID: 29471284

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Project description:Today, many contaminants of emerging concern can be measured in waters across the United States, including the tributaries of the Great Lakes. However, just because the chemicals can be measured does not mean that they necessarily result in harm to fish and other aquatic species. Complicating risk assessment in these waters is the fact that aquatic species are encountering the chemicals as mixtures, which may have additive or synergistic risks that cannot be calculated using single chemical hazard and concentration-response information. We developed an in vitro effects-based screening approach to help us predict potential liver toxicity and cancer in aquatic organisms using water from specific Great Lakes tributaries: St. Louis River (MN), Bad River (WI), Fox River (WI), Manitowoc River (WI), Milwaukee River (WI), Indiana Harbor Canal (IN), St. Joseph River (MI), Grand River (MI), Clinton River (MI), River Rouge (MI), Maumee River (OH), Vermilion River (OH), Cuyahoga River (OH), Genesee River (NY), and Oswego River (NY). We exposed HepG2 cells for 48hrs to medium spiked with either field collected water (final concentration of environmental samples in the exposure medium were 75% of the field-collected water samples) or purified water. Using a deep neural network we clustered our collection sites from each tributary based on water chemistry. We also performed high throughput transcriptomics on the RNA obtained from the HepG2 cells. We used the transcriptomics data with our Bayesian Inferene for Sustance and Chemical Toxicity (BISCT) Bayesian Network for Steatosis to predict the probability of the field samples yielding a gene expression pattern consistent with predicting steatosis as an outcome. Surprisingly, we found that the probability of steatosis did not correspond to the surface water chemistry clustering. Our analysis suggests that chemical signatures are not informative in predicting biological effects. Furthermore, recent reports published after we obtained our samples, suggest that chemical levels in the sediment may be more relevant for predicting potential biological effects in the fish species developing tumors in the Great Lakes basin.

Project description:We previously reported the bioaccumulation of contaminants of emerging concern (CECs), including pharmaceuticals and personal care products (PPCPs) and perfluorinated compounds, in field-collected juvenile Chinook salmon from urban estuaries of Puget Sound, WA (Meador et al., 2016). Although the toxicological impacts of CECs on salmon are poorly understood, several of the detected contaminants disrupt mitochondrial function in other species. Here, we sought to determine whether environmental exposures to CECs are associated with hepatic mitochondrial dysfunction in juvenile Chinook. Fish were exposed in the laboratory to a dietary mixture of 16 analytes representative of the predominant CECs detected in our field study. Liver mitochondrial content was reduced in fish exposed to CECs, which occurred concomitantly with a 24-32% reduction in expression of peroxisome proliferator-activated receptor (PPAR) Y coactivator-1a (pgc-1?), a positive transcriptional regulator of mitochondrial biogenesis. The laboratory exposures also caused a 40-70% elevation of state 4 respiration per unit mitochondria, which drove a 29-38% reduction of efficiency of oxidative phosphorylation relative to controls. The mixture-induced elevation of respiration was associated with increased oxidative injury as evidenced by increased mitochondrial protein carbonyls, elevated expression of glutathione (GSH) peroxidase 4 (gpx4), a mitochondrial-associated GSH peroxidase that protects against lipid peroxidation, and reduction of mitochondrial GSH. Juvenile Chinook sampled in a WWTP effluent-impacted estuary with demonstrated releases of CECs showed similar trends toward reduced liver mitochondrial content and elevated respiratory activity per mitochondria (including state 3 and uncoupled respiration). However, respiratory control ratios were greater in fish from the contaminated site relative to fish from a minimally-polluted reference site, which may have been due to differences in the timing of exposure to CECs under laboratory and field conditions. Our results indicate that exposure to CECs can affect both mitochondrial quality and content, and support the analysis of mitochondrial function as an indicator of the sublethal effects of CECs in wild fish.

Dataset Information

Adverse metabolic effects in fish exposed to contaminants of emerging concern in the field and laboratory.

Publications

Adverse metabolic effects in fish exposed to contaminants of emerging concern in the field and laboratory.

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