Copper and Temperature Interactions Induce Differential Physiological and Metal Exclusion Responses in the Model Brown Macroalga Ectocarpus

Abstract

The toxic effects of copper (Cu) excess in brown macroalgae have been well characterized. However, the interactive effects of increased temperatures, associated with climate change, and Cu stress on these macrophytes remain almost unexplored. In this study, we exposed the model brown seaweed Ectocarpus to different Cu concentrations (0, 0.8, 1.6, and 3.2 μM) at two different temperatures (15 and 25 °C). Relative growth rates decreased at 25 °C for the two highest Cu concentrations after 8 days of exposure, but a contrasting pattern was observed in the photosynthetic maximum quantum yield (F_v/F_m) and photosynthetic efficiency (α), where reductions were observed at 15 °C for the same Cu concentrations. Although no differences among treatments were observed for chlorophyll a (Chla) and chlorophyll c (Chlc), a reduction in concentration of the accessory pigment fucoxanthin (Fx) was only observed at 15 °C in all Cu treatments. Interestingly, at 25 °C, 20.1% less total Cu (intracellular + extracellularly bound) accumulated compared to 15 °C upon exposure to 3.2 μM Cu. Likewise, 33.1 and 23.8% less Cu accumulated intracellularly at 25 °C after exposure to 1.6 μM and 3.2 μM Cu, respectively. Additionally, at 25 °C about half of the Cu ions accumulated intracellularly and half extracellularly compared to 15 °C, where Cu accumulated mostly intracellularly at the two highest Cu concentrations. The results presented here provide valuable information to better understand the interactive effects of increased temperature and excess Cu in the stress response of Ectocarpus, suggesting that increased temperature helps to offset the negative impacts of exposure to high Cu concentrations.

Keywords: chlorophyll a fluorescence; climate change; rapid light curves; seaweed; trace metals.

Figure 1

Relative growth rates (RGRs) of Ectocarpus exposed to combinations of one of four Cu concentrations (0, 0.8, 1.6, and 3.2 μM) and one of two temperatures (15 °C and 25 °C) for 8 days. Asterisks (*) indicate significant differences (p < 0.05) found after Tukey’s test for factor ‘temperature’. Error bars represent ± 1 SD, n = 3.

Figure 2

Photosynthetic parameters: (a) F_v/F_m: maximum quantum yield, (b) α: efficiency of light captured for photosynthesis, (c) ETR_max: maximum electron transport rate, (d) E_k: minimum saturating irradiance, (e) NPQ_max: maximal non-photochemical quenching, obtained from rapid light curves (RLCs) in Ectocarpus exposed to combinations of four Cu concentrations (0, 0.8, 1.6, and 3.2 μM) and two temperatures (15 °C and 25 °C) for 6 days. Asterisks (*) indicate significant differences (p < 0.05) found after Tukey’s test for factor ‘temperature’ within Cu concentration, and crosses (+) for factor ‘copper’ within temperature. Error bars indicate ± 1 SD, n = 3.

Figure 3

Concentrations of Chla, Chlc, and Fx in Ectocarpus exposed to a combination of one of four Cu concentrations (0, 0.8, 1.6, and 3.2 μM) and one of two temperatures (15 °C and 25 °C) for 6 days. Asterisks (*) indicate significant reductions in Fx content (p < 0.05) found after Tukey’s test for factor ‘temperature’ and crosses (+) for factor ‘copper’. Error bars indicate ± 1 SD, n = 3.

Figure 4

Total (a) and intracellular (b) copper accumulation in Ectocarpus exposed to combinations of one of four Cu concentrations (0, 0.8, 1.6, and 3.2 μM) and one of two temperatures, 15 °C and 25 °C, for 6 days. Asterisks (*) indicate significant differences (p < 0.05) found after Tukey’s test for factor ‘temperature’ within Cu concentration and crosses (+) for factor ‘copper’ within temperature. Error bars indicate ± 1 SD, n = 3.