Physiological responses of chlorophyta microalgae under environmentally relevant copper concentrations: biomolecules, oxidative stress and photosynthesis

Abstract

Microalgae require copper (Cu) in trace levels for their growth and metabolism. It is a vital component of certain metalloproteins, participates in the photosynthetic process, and catalyzes various redox reactions. Although this element has been widely studied concerning microalgae physiology, the effects of environmentally relevant levels have been less investigated. The aim of this study was to see the effect of environmental copper concentrations on some aspects of algae physiology, as growth rates, biomolecules (carbohydrates, lipids, proteins, and pigments) production, antioxidant response, and photosynthesis. For this, Ankistrodesmus flexuosus, Curvastrum pantanale, Monoraphidium sp., and Chlamydomonas chlorastera were the test organisms. They were kept under laboratory controlled conditions with Cu concentrations ranging from low (0.1 nM) to high (5480.0 nM) free Cu ions (Cu2+). Cultures lasted 96 h and all analyses were done in exponential growth phase. Cell densities and growth rates were unaffected in low Cu concentrations up to, 9.1 nM Cu2+ in C. chlorastera and 7.4 nM Cu2+ in the other species. In relation to pigments, β-carotene and lutein increased in C. chlorastera (1.2 mg g-1 β-carotene; 6.14 mg g-1 lutein) in 0.3–0.4 nM Cu2+. C. chlorastera had the highest, carbohydrates (> 50 pg cell-1) across all Cu concentrations tested, proteins content (270.2 pg cell-1; 0.3 nM Cu2+), and lipids (61.9% dw; 1.2 nM Cu2+). The activities of α, α-diphenyl-β-picrylhydrazyl (DPPH) radical, Glutathione S-transferase (GST), peroxidase (POD), superoxide dismutase (SOD) and malondialdehyde (MDA) content were not affected by low Cu exposure, but increased in high Cu. The microalgae effective quantum yields (ΔF⁄F_m') were more sensitive to Cu than their maximum quantum yields (F_v⁄F_m ). In Monoraphdium sp., Cu increase (3.4–7.4 nM Cu2+) increased photosynthesis, as recorded in the effective quantum yield (ΔF⁄F_m'), relative maximum electron transport rate (rETRm), saturation irradiance (Ek), and photochemical quenching (qP and qL). The non-photochemical quenching (NPQ) and PSII antenna size of Monoraphidium sp. increased in high Cu. Monoraphidium sp. also had the lowest photoinhibition (β) under high irradiance across all Cu exposures. The primary productivity of Monoraphidium sp. was unaltered in low Cu (1.7–21.4 nM Cu2+), but reduced by high Cu (589.0 nM Cu2+). Cu-elicited hormetic responses were seen in lipids content in C. chlorastera, and in photosynthesis in Monoraphidium sp. These findings show that depending on the species and concentration, Cu can stimulate biomolecules accumulation and increase photosynthesis in microalgae, without reducing growth.