Transcriptional response of yellow perch to changes in ambient metal concentrations - a reciprocal field transplantation experiment

Our main objectives wereto investigate the molecular mechanisms involved in metal toxicity and detoxification in the field using juvenile yellow perch subjected to differents levels of this metal exposure. Recent local adaptation to pollution has been evidenced in several organisms inhabiting environments heavily contaminated by metals. Nevertheless, the molecular mechanisms underlying adaptation to high metal concentrations are poorly understood, especially in fishes. Yellow perch (Perca flavescens) populations from lakes in the mining area of Rouyn-Noranda (QC, Canada) have been faced with metal contamination for about 90 years. Here, we examine gene transcription patterns of fish reciprocally transplanted between a reference and a metal-contaminated lake and also fish caged in their native lake. After four weeks, 111 genes were differentially transcribed in metal-naïve fish transferred to the metal-contaminated lake, revealing a plastic response to metal exposure. Genes involved in the citric cycle and beta-oxidation pathways were under-transcribed, suggesting a potential strategy to mitigate the effects of metal stress by reducing energy turnover. However, metal-contaminated fish transplanted to the reference lake did not show any transcriptomic response, indicating a reduced plastic response capability to sudden reduction in metal concentrations. Moreover, the transcription of other genes, especially ones involved in energy metabolism, was affected by caging. Overall, our results highlight environmental stress response mechanisms in yellow perch at the transcriptomic level and support a rapid adaptive response to metal exposure through genetic assimilation. Comparison between fish Op and Op→Op using a pairwise design corresponding to the cage experiment in the reference lake Opasatica (Op), comparison between fish Du and Du→Du using a pairwise design corresponding to the cage experiment in the metal contaminated lake Dufault (Du), comparison between fish from reference lake transplanted to the metal contaminated lake (Op→Du) and fish from reference lake caged in their own lake (Op→Op) using pairwise design corresponding to the experiment of metal contamination, comparison between fish from metal contaminated lake transplanted to the reference lake (Du→Op) and fish from the metal contaminated lake caged in their own lake (Du→Du) using pairwise design corresponding to the depuration experiment.

本研究的核心目标为探究野外环境下金属毒性与解毒作用相关的分子机制，实验对象为暴露于不同浓度该金属的幼年黄鲈（yellow perch）。已有研究证实，栖息于重金属重度污染环境中的多种生物，已对污染产生了近期的本地适应性演化。然而，当前学界对高浓度金属暴露下适应性演化的分子机制仍知之甚少，在鱼类类群中尤为突出。栖息于加拿大魁北克省鲁安-诺兰达（Rouyn-Noranda）矿区周边湖泊的黄鲈（Perca flavescens）种群，已暴露于金属污染环境长达约90年。本研究分析了参照湖与金属污染湖之间互置移植的幼鲈，以及原位网箱养殖的幼鲈的基因转录模式。暴露养殖4周后，移植至金属污染湖的未接触金属幼鲈体内共有111个基因出现差异转录，表明其对金属暴露存在可塑性响应。参与柠檬酸循环（citric cycle）与β-氧化（beta-oxidation）通路的基因转录水平出现下调，提示幼鲈可能通过降低能量代谢周转，以缓解金属胁迫带来的损伤。但移植至参照湖的污染适应性幼鲈未表现出任何转录组响应，表明其对金属浓度骤降的可塑性响应能力已出现衰退。此外，网箱养殖环境亦会影响部分基因的转录水平，其中尤以能量代谢相关基因为甚。综上，本研究结果从转录组层面揭示了黄鲈应对环境胁迫的分子机制，并证实其可通过遗传同化（genetic assimilation）快速产生对金属暴露的适应性响应。本研究采用配对设计开展四组比较分析：分别为参照湖奥帕萨蒂卡（Opasatica, Op）的原位网箱养殖幼鲈（Op组）与本湖原位网箱的同种群幼鲈（Op→Op组，对应奥帕萨蒂卡湖原位网箱实验）；金属污染湖杜福尔（Dufault, Du）的原位网箱养殖幼鲈（Du组）与本湖原位网箱的同种群幼鲈（Du→Du组，对应杜福尔湖原位网箱实验）；移植至金属污染湖的参照湖幼鲈（Op→Du组）与本湖原位网箱的参照湖幼鲈（Op→Op组，对应金属暴露实验）；以及移植至参照湖的污染湖幼鲈（Du→Op组）与本湖原位网箱的污染湖幼鲈（Du→Du组，对应净化实验）。