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Effect of contaminants of emerging concern on liver mitochondrial function in Chinook salmon.

ABSTRACT: 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.

SUBMITTER: Yeh A

PROVIDER: S-EPMC5590637 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Effect of contaminants of emerging concern on liver mitochondrial function in Chinook salmon.

Yeh Andrew A Marcinek David J DJ Meador James P JP Gallagher Evan P EP

Aquatic toxicology (Amsterdam, Netherlands) 20170616

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 exp ...[more]

PMID: 28668760

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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:The Columbia River and its tributaries provide essential spawning and rearing habitat for many salmonid species, including Chinook salmon (Oncorhynchus tshawytscha). Chinook salmon were historically abundant throughout the basin and Native Americans in the region relied heavily on these fish for thousands of years. Following the arrival of Europeans in the 1800s, salmon in the basin experienced broad declines linked to overfishing, water diversion projects, habitat destruction, connectivity reduction, introgression with hatchery-origin fish, and hydropower development. Despite historical abundance, many native salmonids are now at risk of extinction. Research and management related to Chinook salmon is usually explored under what are termed "the four H's": habitat, harvest, hatcheries, and hydropower; here we explore a fifth H, history. Patterns of prehistoric and contemporary mitochondrial DNA variation from Chinook salmon were analyzed to characterize and compare population genetic diversity prior to recent alterations and, thus, elucidate a deeper history for this species. A total of 346 ancient and 366 contemporary samples were processed during this study. Species was determined for 130 of the ancient samples and control region haplotypes of 84 of these were sequenced. Diversity estimates from these 84 ancient Chinook salmon were compared to 379 contemporary samples. Our analysis provides the first direct measure of reduced genetic diversity for Chinook salmon from the ancient to the contemporary period, as measured both in direct loss of mitochondrial haplotypes and reductions in haplotype and nucleotide diversity. However, these losses do not appear equal across the basin, with higher losses of diversity in the mid-Columbia than in the Snake subbasin. The results are unexpected, as the two groups were predicted to share a common history as parts of the larger Columbia River Basin, and instead indicate that Chinook salmon in these subbasins may have divergent demographic histories.

Dataset Information

Effect of contaminants of emerging concern on liver mitochondrial function in Chinook salmon.

Publications

Effect of contaminants of emerging concern on liver mitochondrial function in Chinook salmon.

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