Effects of chronic exposure to dietary selenomethionine on the physiological stress response in juvenile white sturgeon (Acipenser transmontanus)
Introduction
Selenium (Se) is an essential micronutrient required by all vertebrate species for incorporation into selenoproteins. However, there is a fine line between Se essentiality and toxicity (Janz, 2011, Lemly, 1997). Dietary requirements for maintaining normal physiological function range between 0.1 and 0.5 μg Se/g dry mass (dm) in fish, but studies have shown concentrations >3 μg Se/g dm in the diet can result in toxicity (Hamilton, 2004, Lemly, 1997). Inorganic Se is the most prevalent form found in surface waters, where it is rapidly bioaccumulated and biotransformed by microorganisms into organoselenides, such as selenomethionine (SeMeth). These organoselenides are transferred up the food chain to more sensitive, higher trophic level organisms (Janz, 2011, Stewart et al., 2010). SeMeth is the major dietary form of Se that aquatic organisms are exposed to and is of particular concern because it is known to persist and bioaccumulate through the food chain (Lemly and Smith, 1987).
There is significant concern about the effects of Se contamination on aquatic vertebrates, including fish. Among these, white sturgeon (WS) are of great interest because their longevity and benthic lifestyle make them more susceptible to exposure and bioaccumulation than other fish species (Little et al., 2012, Vardy et al., 2011, Vardy et al., 2013). In particular, populations of WS in the Kootenay River and San Francisco (S.F.) Bay-Delta are at risk of exposure to Se because of increasing Se inputs into these ecosystems (Presser and Luoma, 2006, Dessouki and Ryan, 2010). Se concentrations up to 12 μg/g, which exceed the toxic effect threshold recommended by Lemly (2002) and approach the US Environmental Protection Agency’s (EPA) criterion of 15.1 mg/kg (USEPA, 2016), were detected in ovarian tissue from Kootenai River WS (Kruse and Scarnecchia, 2002). Water quality monitoring has also shown total Se concentrations in the Kootenay River are increasing at a rate of 0.012 μg/L per year, and these increases are potentially associated with upstream inputs from open-pit coal mining operations. If these rates continue, Se concentrations are expected to exceed the current CCME water quality guideline (1 μg/L) within 15–32 years (Dessouki and Ryan, 2010). Concerns about concentrations of Se in the S.F. Bay-Delta originate from effluent discharge from oil refineries in the Bay area and agriculture drainage from the San Joaquin Valley. Although total dissolved Se concentrations in the S.F. Bay-Delta are below water quality criteria (1 μg/L), WS have been found to contain concentrations up to 15 and 30 μg Se/g dm in their muscle and liver tissue, respectively (White et al., 1988, Urquhart and Rigalado, 1991, Linville et al., 2002, Linares-Casenave et al., 2014), and these concentrations are greater than the fish tissue criteria set by the US EPA (USEPA, 2016). Sturgeon in the S.F. Bay-Delta feed primarily on filter feeding bivalves (eg. Potamocorbula amurensis), which readily accumulate Se. P. amurensis have been found to contain up to 20 μg Se/g dm (Linville et al., 2002), which is greater than the interim chronic dietary guideline suggested for fish (4 μg Se/g dm) (Beatty and Russo, 2014) and Presser and Luoma (2006) predicted Se concentrations in bivalves could reach >100 μg/g dm under certain Se loading scenarios. Without remediation and management of Se inputs, there is an increased risk of dietary intake, bioaccumulation and toxicity in local sturgeon populations (Presser and Luoma, 2006).
Recently, studies have examined the sensitivity of juvenile WS chronically exposed to SeMeth through the diet (Linville, 2006, Tashjian et al., 2006, De Riu et al., 2014, Zee et al., 2016a). Adverse effects on growth rate, activity and feeding behavior were observed in juvenile WS exposed to concentrations of SeMeth >40 μg/g (Linville, 2006, Tashjian et al., 2006, De Riu et al., 2014, Zee et al., 2016a). Exposure to concentrations >20 μg Se/g caused histopathological lesions in the kidneys, livers and gills (Linville, 2006, Tashjian et al., 2006, De Riu et al., 2014, Zee et al., 2016a), and a significant increase in the prevalence of mild to moderate edema was observed at dietary concentrations as low as 5.6 μg Se/g (Zee et al., 2016a). Increased whole body moisture content and decreased lipid and energy content also were observed in WS fed concentrations >40 μg Se/g (Tashjian et al., 2006, De Riu et al., 2014). These findings suggest that energy homeostasis in juvenile WS is impacted by dietary SeMeth exposure, and further investigation is warranted. Altered energy homeostasis could also indicate an effect on the physiological stress response.
Se exposure has been shown to affect the physiological stress response and energy homeostasis in several species of teleost fish (Miller et al., 2007, Miller et al., 2009, Miller and Hontela, 2011, Thomas and Janz, 2011, Wiseman et al., 2011, McPhee and Janz, 2014). Rainbow trout chronically exposed to dietary SeMeth (8.47 mg/kg dm) were found to have elevated levels of plasma cortisol and were unable to mount a cortisol response when subjected to an acute handling stressor (Wiseman et al., 2011). The exposed trout also had a significantly greater hepatic somatic index (HSI), body mass and condition factor, as well as increased concentrations of glycogen and triglycerides in the muscle. However, glycogen and triglyceride concentrations decreased 24 h after the handling stressor (Wiseman et al., 2011). Zebrafish fed >26.6 μg Se/g had elevated cortisol levels, as well as altered swim performance and significant increases in energy stores (triglycerides and glycogen) when fed >3.7 μg Se/g (Thomas and Janz, 2011). Fathead minnows fed >5.4 μg Se/g had significantly elevated whole body triglyceride concentrations and decreased whole body glycogen concentrations compared to controls (McPhee and Janz, 2014).
Although previous studies showed effects of SeMeth on the physiological stress response and energy homeostasis in teleost species (Thomas and Janz, 2011, Wiseman et al., 2011, McPhee and Janz, 2014), these effects are not known in WS. Therefore, the objective of this study was to determine the potential effects of chronic dietary SeMeth exposure on the physiological stress response in juvenile WS. Sturgeon with an altered stress response and impaired energy homeostasis could have a reduced ability to feed, avoid predators, swim upstream for spawning and cope with other secondary stressors, which would be detrimental to the survival of an already endangered species (Tashjian et al., 2006).
This study was informed by Zee et al. (2016a) and aimed to characterize impacts on the stress response and energy homeostasis as an explanation for the severe pathologies reported in the previous study, while oxidative stress was discussed as a potential driver of Se toxicity in Zee et al. (2016b). Together these studies will provide further insight into the sensitivity of juvenile white sturgeon to dietary SeMeth and the mechanism(s) leading to toxicity.
Section snippets
Test chemical and species
Seleno-l-methionine (SeMeth)(purity >98%) was purchased from Sigma-Aldrich (Oakville, ON, Canada). WS were reared in the Aquatic Toxicology Research Facility (ATRF) at the University of Saskatchewan, from eggs donated by the Kootenay Trout Hatchery (Fort Steele, BC, Canada), until they were approximately 3 yr old (124 ± 8.6 g wet mass [mean ± S.E.M]). Sturgeon cultures were maintained at approximately 12 °C, in 712 L flow-through tanks, that were continuously supplied with dechlorinated City of
Selenium analysis, edema, and mortality
Total selenium concentrations in control feed and feed spiked with the low, medium and high amounts of SeMeth were 1.4 ± 0.02, 5.6 ± 0.01, 22.4 ± 0.26 and 104.4 ± 2.78 μg Se/g dm (mean ± S.E.M.), respectively, as described in Zee et al. (2016a). Concentrations of Se in the spiked feed were significantly greater than those in control feed (p < 0.05).
Tissue concentrations of Se increased with increasing dietary concentrations of Se. Specifically, on day 72, total Se concentrations in the muscle tissue of
Discussion
Results from this study suggest dietary exposure to >22.4 μg Se/g dm can affect cortisol dynamics and mobilization of energy substrates in juvenile WS. Changes in cortisol dynamics can negatively affect energy metabolism in fish and lead to a depletion of energy available for normal physiological function, and ultimately affect fish health and survival (Wedemeyer and McLealy, 1981). Chronic exposure to 104.4 μg Se/g dm, under basal conditions, altered plasma levels of cortisol, glucose and
Acknowledgements
This work was supported through the Canada Research Chair program and an NSERC Discovery grant to M. Hecker. The authors wish to thank Jason Raine for use of the Aquatic Toxicology Research Facility (ATRF) at the Toxicology Centre, University of Saskatchewan. The authors would also like to thank Bryanna Eisner, Danielle Gagnon, Brett Tendler, Shawn Beitel, Jon Doering and Michelle Podaima for assistance in the study, as well as Lucy Kapronczai and Jith Thomas for their assistance with plasma
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