Assessing Cu impacts on freshwater diatoms: biochemical and metabolomic responses of Tabellaria flocculosa (Roth) Kützing

Abstract

Metals are a recognised threat to aquatic organisms but the impact of metals such as copper (Cu) on benthic freshwater diatoms is poorly understood, even if diatoms are commonly used as water quality indicators. Our study aimed to elucidate the cellular targets of Cu toxicity and the mechanisms cells resort to counteract toxicity and to increase tolerance to Cu. A concerted approach analysing the biochemical, physiological and metabolome alterations in diatom cells was conducted by exposing the freshwater diatom Tabellaria flocculosa to 0, 0.3, 6 and 10μgCu/L. Cu was already toxic to T. flocculosa at concentrations common in environments and which are not usually considered to be contaminated (0.3μgCu/L). Under Cu impact, the metabolome of T. flocculosa changed significantly, especially at high concentrations (6 and 10μgCu/L). Cu toxicity was counteracted by increasing extracellular immobilization (EPS, frustulins), antioxidant (SOD, CAT) and detoxifying (GSTs) enzymes activity and low molecular weight antioxidants (GSH). These mechanisms were fuelled by higher energy production (increased ETS activity). At the highest Cu concentration (10μg/L), these processes were specially enhanced in an attempt to restrain the oxidative stress generated by high intracellular Cu concentrations. However, these mechanisms were not able to fully protect cells, and damage in membranes and proteins increased. Moreover, the decrease of hydroxylamine and unsaturated fatty acids and the increase of saturated fatty acids, 2-palmitoylglycerol, glycerol and diterpenoid compounds should be tested as new specific markers of Cu toxicity in future studies. This information can support the prediction of diatom behaviour in different Cu contamination levels, including highly impacted environments, such as mining scenarios, and may assist in environmental risk assessment policies and restoration programs.

Copper Affects Composition and Functioning of Microbial Communities in Marine Biofilms at Environmentally Relevant Concentrations

“…These findings agree with previous results of (Gustavson et al, 1999), who also reported an increase of centric Bacillariophyta in marine phytoplankton as a consequence of Cu exposure. The Cu tolerance in diatoms has been linked with their capacity to synthetize extracellular polysaccharides and frustuline (Gonçalves et al, 2018). Nevertheless, previously published mesocsom studies also provide a partly conflicting picture of diatom tolerance to Cu.…”

“…Cu is an essential element (Festa and Thiele, 2011), but becomes toxic at higher concentrations (Amara et al, 2018), depending on metal speciation, accumulation (Meylan et al, 2004; Serra et al, 2009) and exposed organism (Barranguet et al, 2003; Amara et al, 2018). In photosynthetically active cells Cu inhibits CO 2 fixation and PSII activity (Pandey et al, 1992), causes oxidative stress and ultimately inhibits cell growth (Gonçalves et al, 2018). In bacteria, Cu affects various cellular enzymes and proteins involved in energy metabolism (Waldron et al, 2009).…”

Metabolomic Responses of Green Alga Chlamydomonas reinhardtii Exposed to Sublethal Concentrations of Inorganic and Methylmercury

“…57 However, the present findings for IHg and MeHg are opposite to the decrease of some of the amino acids (lysine, arginine, and glutamine) observed in copper exposure of other green algae Chlorella sp., 58,59 Scenedesmus quadricauda, 60 and diatom Tabellaria flocculosa (Roth) Kuẗzing. 61 Nucleobase/-Tide/-Side Metabolism. The metabolism of both pyrimidine and purine derivatives was significantly affected in algae exposed to IHg and MeHg ( Figures S7 and S8).…”

Marine Antibiofouling Properties of TiO2 and Ti-Cu-O Films Deposited by Aerosol-Assisted Chemical Vapor Deposition

“…Indeed, they produce extracellular polysaccharides (EPS) to immobilize metals outside the cells, such as copper. As a result, the excretion of these protective products reduces sensitivity to copper exposure [71][72][73]. So the more copper there is (up to a certain point whereat the concentration of metal is too high to be countered), the more EPS there are, and the more diatoms adhere strongly to the substratum.…”