1 INTRODUCTION

Zooplankton such as copepods occupy an intermediate trophic position in the aquatic food web of most lake ecosystems (Lampert & Sommer, 2007). They inhabit lakes with a broad range of physicochemical and optical properties and are thus exposed to a variety of environmental threats and stressors that require specific responses. To survive and succeed under highly variable conditions, the animals adjust e.g. their biochemistry, physiology, morphology, behaviour, or life history (DeWitt et al., 1998; West-Eberhard, 2003). On the smallest timescale, organisms activate an array of immediate stress responses (Lauritano et al., 2012).

Physiological adjustments are of particular importance in harsh environments such as alpine lakes (i.e., located above tree line), where plankton organisms face oligotrophy, low temperatures, and strong seasonal contrasts. Their number currently increases rapidly in mountain areas such as the Alps due to glacier retreat (Mölg et al., 2021), a phenomenon observed worldwide (Carrivick & Tweed, 2013). Newly formed lakes and those fed by glacial meltwaters show significant levels of turbidity, although these lakes will eventually turn clear when the hydrological connectivity to the glacier is lost (Desloges, 1994; Vinebrooke et al., 2010). Climate change-induced shorter periods of ice cover will lead to earlier exposure to high levels of solar ultraviolet radiation (UVR) (Adrian et al., 2009), which significantly structures ecosystem processes in clear alpine lakes (Rose et al., 2009; Sommaruga, 2001). However, in the presence of glacier-derived turbidity, the UVR threat is strongly reduced via attenuation of solar radiation (Rose et al., 2014; Tartarotti et al., 2017).

We have recently shown that copepods rely on a combination of behavioural and physiological strategies when lakes shift from glacially turbid to clear conditions (Tartarotti et al., 2017). In clear lakes, the highly energetic short wavelengths of solar UVR penetrate deep into the water column, resulting in potentially harmful effects on aquatic biota (see Rautio & Tartarotti, 2010 for a review).

In habitats where zooplankton cannot avoid hazardous radiation intensities, they rely on the accumulation of photoprotective compounds such as mycosporine-like amino acids (MAAs) that directly screen UVR (Karentz et al., 1991) or antioxidants such as carotenoids that protect the cells by quenching reactive oxygen species (Cockell & Knowland, 1999). High concentrations of MAAs in alpine copepods (Persaud et al., 2007; Tartarotti et al., 2001; Tartarotti et al., 2004; Tartarotti et al., 2017) and their relation to lake elevation and UVR transparency (Tartarotti et al., 2001, 2004, 2017) support the idea that MAAs are essential for the survival of these organisms. The accumulation of carotenoids in copepods, a widely observed phenotypic adaptation, has also been linked to UVR-induced photoprotection (Hairston Jr., 1979; Hansson, 2000; Ringelberg et al., 1984; Sommaruga, 2010; Tartarotti et al., 2018). However, observations in low-UVR environments suggest that other factors such as reproduction and lipid metabolism may also control carotenoid accumulation (Schneider et al., 2012; Schneider et al., 2016; Sommer et al., 2006). Previous studies in clear lakes have revealed seasonal patterns underlying copepod content of MAAs and carotenoids (Moeller et al., 2005; Tartarotti et al., 2018; Tartarotti & Sommaruga, 2006). However, whereas MAAs concentrations are higher in copepods from clear than from turbid alpine lakes (i.e., positively linked to UVR exposure), carotenoid contents do not necessarily differ and may even show the opposite trend (Tartarotti et al., 2017).

As key components of the cellular stress response, heat shock proteins act as molecular chaperones and in the recovery of cells from stress by maintaining the integrity of cellular proteins (Feder & Hofmann, 1999; Sørensen et al., 2003). In aquatic organisms, a wide array of environmental challenges, ranging from thermal, oxidative, chemical to UVR stress, induces the expression of stress proteins (Feder & Hofmann, 1999; Sanders, 1993; Tomanek, 2010). Induction of hsp genes after exposure to UVR was observed in marine copepods (Kim et al., 2015; Won et al., 2015) and was found to be species- as well as gene-specific (Han et al., 2016). Less information is available for freshwater copepods, but, recently, we have shown that the seasonal plasticity in photoprotection modulates UV-induced hsp gene expression in cyclopoid copepods (Tartarotti et al., 2018). In the clear study lake, the highest expression levels (hsp70) were observed at times of low photoprotection (i.e., ice cover season).

Previous studies with freshwater copepods have found that not only the content of photoprotective compounds (Tartarotti et al., 2017), but also the levels of stress protein genes (hsp60, hsp70, and hsp90) (Tartarotti et al., 2019) differ in populations from either clear or glacially turbid lakes. Here, our aim was to test whether gene expression patterns vary within the same species but in populations from different environments when experimentally exposed to ecologically relevant levels of UVR. We sampled zooplankton from two alpine lakes differing largely in their physicochemical characteristics during summer and autumn to assess population-specific and temporal variation in photoprotection levels and to determine how stressful UVR is using hsp gene expression as a proxy for stress.

中文翻译：

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桡足类在清澈和冰川混浊湖中对紫外线辐射胁迫的表型和分子反应

1 简介

桡足类等浮游动物在大多数湖泊生态系统的水生食物网中占据中间营养位置（Lampert & Sommer,  2007）。它们栖息在具有广泛物理化学和光学特性的湖泊中，因此面临各种需要特定反应的环境威胁和压力源。为了在高度可变的条件下生存和成功，动物会调整它们的生物化学、生理学、形态学、行为或生活史（DeWitt 等人，  1998 年；West-Eberhard，  2003 年）。在最小的时间尺度上，生物体会激活一系列即时应激反应（Lauritano 等人，  2012 年）。

生理调整在高山湖泊（即位于树线以上）等恶劣环境中尤为重要，在这些环境中，浮游生物面临贫营养、低温和强烈的季节对比。由于冰川退缩，它们的数量目前在阿尔卑斯山等山区迅速增加（Mölg 等人，  2021 年），这是一种在全球范围内观察到的现象（Carrivick 和 Tweed，  2013 年）。新形成的湖泊和由冰川融水补给的湖泊显示出明显的浑浊度，尽管当与冰川的水文连通性消失时，这些湖泊最终会变清（Desloges，  1994 年；Vinebrooke 等人，  2010 年））。气候变化引起的较短冰盖期将导致更早暴露于高水平的太阳紫外线辐射 (UVR) (Adrian et al.,  2009 )，这显着构建了清澈高山湖泊中的生态系统过程 (Rose et al.,  2009 ;索马鲁加，  2001 年）。然而，在存在冰川产生的浊度的情况下，UVR 威胁通过太阳辐射的衰减而大大降低（Rose 等人，  2014 年；Tartarotti 等人，  2017 年）。

我们最近表明，当湖泊从冰川混浊转变为清澈条件时，桡足类依赖于行为和生理策略的结合（Tartarotti 等人，  2017 年）。在清澈的湖泊中，太阳 UVR 的高能短波长深入水柱，对水生生物群造成潜在的有害影响（参见 Rautio 和 Tartarotti，  2010 年的综述）。

在浮游动物无法避免危险辐射强度的栖息地，它们依赖于光保护化合物的积累，例如直接屏蔽 UVR（Karentz 等人，  1991）的类霉菌素氨基酸 (MAA) 或通过以下方式保护细胞的类胡萝卜素等抗氧化剂。淬灭活性氧（Cockell & Knowland，  1999 年）。高山桡足类中高浓度的 MAA（Persaud 等人，  2007 年；Tartarotti 等人，  2001 年；Tartarotti 等人，  2004 年；Tartarotti 等人，  2017 年）及其与湖泊高程和 UVR 透明度的关系（Tartarotti 等人。 ,  2001 , 2004 , 2017) 支持 MAA 对这些生物的生存至关重要的观点。桡足类中类胡萝卜素的积累是一种广泛观察到的表型适应，也与 UVR 诱导的光保护有关（Hairston Jr.,  1979 ; Hansson,  2000 ; Ringelberg et al.,  1984 ; Sommaruga,  2010 ; Tartarotti et al.,  2018）。然而，在低 UVR 环境中的观察表明，生殖和脂质代谢等其他因素也可能控制类胡萝卜素的积累（Schneider 等人，  2012；Schneider 等人，  2016；Sommer 等人，  2006）。先前在清澈湖泊中的研究揭示了 MAA 和类胡萝卜素桡足类含量的季节性模式（Moeller 等人，  2005 年；Tartarotti 等人，  2018 年；Tartarotti 和 Sommaruga，  2006 年）。然而，尽管来自清澈的桡足类动物的 MAAs 浓度高于来自浑浊的高山湖泊（即，与 UVR 暴露呈正相关），但类胡萝卜素含量不一定不同，甚至可能呈现相反的趋势（Tartarotti 等人，  2017 年）。

作为细胞应激反应的关键成分，热休克蛋白充当分子伴侣，并通过维持细胞蛋白的完整性使细胞从应激中恢复（Feder & Hofmann,  1999 ; Sørensen et al.,  2003）。在水生生物中，从热、氧化、化学到 UVR 应激的各种环境挑战都会诱导应激蛋白的表达（Feder & Hofmann,  1999 ; Sanders,  1993 ; Tomanek,  2010）。在海洋桡足类动物（Kim et al., 2015 ; Won et al.,  2015 ）中观察到暴露于 UVR 后 hsp基因的诱导，并且被发现具有物种特异性和基因特异性（Han et al., 2016 年）。淡水桡足类的可用信息较少，但最近，我们已经表明，光保护中的季节性可塑性调节了旋臂类桡足类中紫外线诱导的hsp基因表达（Tartarotti 等人，  2018 年）。在清澈的研究湖中，在低光保护时间（即冰盖季节）观察到最高表达水平 ( hsp70 )。

先前对淡水桡足类的研究发现，不仅光保护化合物的含量（Tartarotti et al.,  2017），而且应激蛋白基因（hsp60、hsp70和hsp90）的水平（Tartarotti et al.,  2019 ）) 来自清澈或冰川混浊湖泊的种群不同。在这里，我们的目的是测试当实验暴露于生态相关水平的 UVR 时，基因表达模式是否在同一物种内但在来自不同环境的种群中发生变化。我们从两个高山湖泊中采集浮游动物样本，它们在夏季和秋季的物理化学特征差异很大，以评估特定人群和光保护水平的时间变化，并确定 UVR 使用hsp基因表达作为压力代理的压力有多大。