Phenotypic and molecular responses of copepods to UV radiation stress in a clear versus a glacially turbid lake

Abstract

Zooplankton are exposed to multiple environmental stressors in alpine lakes. However, phenotypic and molecular responses of copepods to different environmental conditions, including ultraviolet radiation (UVR), are still not fully understood. Here, we tested whether gene expression patterns vary within the same species, Cyclops abyssorum tatricus, but in populations from different environments (a clear vs. a glacially turbid lake) when exposed to UVR. Moreover, we wanted to examine potential seasonal variation (summer vs. autumn) in copepod gene expression.We measured photoprotective compounds (mycosporine-like amino acids and carotenoids) and antioxidant capacities in two copepod populations and studied gene expression of heat shock proteins (hsps) as indicator of stress after UVR exposure in the laboratory.Compared with the copepod population from the clear lake, the population from the turbid lake showed lower mycosporine-like amino acid, but higher carotenoid concentrations that decreased over the season. Antioxidant capacities (both lipophilic and hydrophilic) were higher in autumn than in summer. The hsp60 and hsp90 genes were constitutively expressed, regardless of habitat origin and season, while hsp70 was upregulated after exposure to UVR (up to 2.8-fold change). We observed stronger upregulation of hsp70 gene expression in autumn for the turbid and summer for the clear lake, with highest gene expression 24 hr post-UVR exposure (up to 10.2-fold change in the turbid and 3.9-fold in the clear lake).We show how variation in phenotypic traits modulates hsp gene expression patterns, specifically hsp70 gene expression. Rapidly induced defences against cellular stress may improve survival in harsh environments such as alpine lakes, especially since these sensitive ecosystems may experience further changes in the future.

Keywords: alpine lakes; glacier retreat; hsp70; photoprotection; zooplankton.

FIGURE 1

Variation of (a) total mean MAA and (b) carotenoid concentrations (μg/mg dry weight [DW]; n = 3), and (c) mean lipophilic (nmol trolox equivalents/mg protein; n = 3) and (d) hydrophilic antioxidant capacity (nmol ascorbic acid equivalents/mg protein; n = 3) in Cyclops abyssorum tatricus from the clear Lake Gossenköllesee in August and end of September 2014 (left; white bars) and from the turbid Lake Faselfadsee 3 in August and October 2014 (right; blue bars). Error bars indicate + SE. Different letters above the bars indicate a significant difference found with two‐way analysis of variance (ANOVA) with interactions followed by a Tukey HSD post hoc test

FIGURE 2

Expression of heat shock protein 70 (hsp70) gene (a), heat shock protein 60 (hsp60) gene (b) and heat shock protein 90 (hsp90) gene (c) in Cyclops abyssorum tatricus from the clear Lake Gossenköllesee in August and end of September 2014. Gene expression was quantified (absolute quantification method) at the beginning of the experiment (t₀), following 6 hr of ultraviolet (UV) radiation exposure with photo‐reactivation radiation (UV), 6 hr of photosynthetically active radiation (PAR), when kept in the dark (d), and 24 hr post‐UV radiation exposure (UV 24 hr); n = 3 biological replicates, 60 copepodid CIII–CV life stages were pooled per sample. Shown are mean ± SE expression. Different letters above the bars indicate a significant difference found with two‐way analysis of variance (ANOVA) with interactions followed by a Tukey HSD post hoc test

FIGURE 3

Expression of heat shock protein 70 (hsp70) gene (a), heat shock protein 60 (hsp60) gene (b) and heat shock protein 90 (hsp90) gene (c) in Cyclops abyssorum tatricus from the turbid Lake Faselfadsee 3 in August and October 2014. Gene expression was quantified (absolute quantification method) at the beginning of the experiment (t ₀), following 6 hr of ultraviolet (UV) radiation exposure with photo‐reactivation radiation (UV), 6 hr of photosynthetically active radiation (PAR), when kept in the dark (d), and 24 hr post‐UV exposure (UV 24 hr, PAR 24 hr, and D 24 hr); n = 3 biological replicates, 60 copepodid CIII–CV life stages were pooled per sample. Shown are mean ± SE expression. Different letters above the bars indicate a significant difference found with two‐way analysis of variance (ANOVA) with interactions followed by a Tukey HSD post hoc test