Department of Integrative Biology, University of Guelph, Guelph, Ontario, Canada.
Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada.
Aquat Toxicol. 2020 Apr;221:105423. doi: 10.1016/j.aquatox.2020.105423. Epub 2020 Jan 23.
Canada's oil sands industry continues to expand and the volume of diluted bitumen (dilbit) transported across North America is increasing, adding to spill risk and environmental contamination. Dilbit exposure is known to cause adverse effects in fish, but linking molecular and cellular changes with ecologically-relevant individual performance metrics is needed to better understand the potential consequences of a dilbit spill into the aquatic environment. Therefore, this study examined the effects of dilbit exposure on subcellular responses in cardiac and skeletal muscle in relation to swimming performance in a migratory fish species at risk of exposure, Atlantic salmon. Smolts were exposed subchronically to environmentally relevant concentrations of the water-soluble fraction of dilbit (WSFd) for 24 d, and then a subset of exposed fish underwent a depuration period of 7 or 14 d, for a total of 3 experimental time points. At each time point, repeat swimming performance was assessed using sequential critical swimming speed tests (U) separated by a 24 h rest period, and then several tissues were collected to determine biotransformation enzyme activation, energetic responses, and gene expression changes. U was unaffected in fish exposed to 67.9 μg/L total initial polycyclic aromatic compounds (PAC), but fish showed a decreased reliance on lipid metabolism for adenosine triphosphate (ATP) in the heart that was maintained through 7 d depuration. In contrast, U increased in fish exposed to 9.65 μg/L PAC, corresponding to an increased reliance on anaerobic metabolic pathways in cardiac and red skeletal muscle, with partial recovery after 7 d depuration. As expected, at both concentrations WSFd hepatic cyp 1A-mediated biotransformation reactions increased, as measured by EROD activity, which remained elevated for 7 d but not after 14 d depuration. Transcript abundance of cyp1a was also increased in muscle tissue and recovered by 14 d depuration. The expression of other stress-related genes increased in white muscle of dilbit-exposed fish, but were largely unchanged in cardiac and red muscle. The transcriptional profile of cardiac tissue was compared to that of sockeye salmon similarly exposed to WSFd in a previous experiment, and is provided in supplemental text. Combined, these results demonstrate that dilbit exposure alters gene expression and enzyme activities related to xenobiotic exposure, cellular stress, and muscle energetics in juvenile Atlantic salmon without impairing swimming performance, and that most of these changes are recoverable within 14 d depuration.
加拿大的油砂产业持续扩张，稀释沥青（dilbit）在北美的运输量不断增加，这增加了溢油风险和环境污染。已证实 dilbit 暴露会对鱼类造成不良影响，但需要将分子和细胞变化与具有生态相关性的个体表现指标联系起来，以便更好地了解 dilbit 溢入水生环境的潜在后果。因此，本研究检测了暴露于 dilbit 对处于溢油风险中的洄游性鱼类——大西洋三文鱼的心脏和骨骼肌亚细胞反应的影响，以及与游泳性能的关系。幼鲑亚慢性暴露于环境相关浓度的 dilbit 水溶性馏分（WSFd）24 天，然后一部分暴露的鱼进行 7 或 14 天的净化期，总共 3 个实验时间点。在每个时间点，使用连续临界游泳速度测试（U）重复评估游泳性能，两次测试之间间隔 24 小时休息期，然后收集几种组织以确定生物转化酶的激活、能量反应和基因表达变化。暴露于 67.9 μg/L 总初始多环芳烃（PAC）的鱼的 U 没有变化，但鱼的心显示出依赖于脂肪代谢产生三磷酸腺苷（ATP）的能力下降，这种下降在 7 天净化期内得以维持。相比之下，暴露于 9.65 μg/L PAC 的鱼的 U 增加，这对应于心脏和红肌中无氧代谢途径的依赖增加，7 天净化后部分恢复。正如预期的那样，在两个浓度下，WSFd 肝 CYP1A 介导的生物转化反应增加，以 EROD 活性衡量，7 天净化后仍保持升高，但 14 天净化后不再升高。肌肉组织中 CYP1A 的转录丰度也增加，并在 14 天净化后恢复。dilbit 暴露的白肌中其他与应激相关的基因表达增加，但心脏和红肌中的变化基本不变。心脏组织的转录谱与之前的实验中同样暴露于 WSFd 的红大麻哈鱼进行了比较，并在补充文本中提供。综合来看，这些结果表明，dilbit 暴露会改变幼大西洋三文鱼的基因表达和与外源性物质暴露、细胞应激和肌肉能量学相关的酶活性，而不会损害游泳性能，并且这些变化中的大多数在 14 天净化期内是可恢复的。
