Heavy metal-induced stress in eukaryotic algae-mechanisms of heavy metal toxicity and tolerance with particular emphasis on oxidative stress in exposed cells and the role of antioxidant response

Abstract

Heavy metals is a collective term describing metals and metalloids with a density higher than 5 g/cm³. Some of them are essential micronutrients; others do not play a positive role in living organisms. Increased anthropogenic emissions of heavy metal ions pose a serious threat to water and land ecosystems. The mechanism of heavy metal toxicity predominantly depends on (1) their high affinity to thiol groups, (2) spatial similarity to biochemical functional groups, (3) competition with essential metal cations, (4) and induction of oxidative stress. The antioxidant response is therefore crucial for providing tolerance to heavy metal-induced stress. This review aims to summarize the knowledge of heavy metal toxicity, oxidative stress and antioxidant response in eukaryotic algae. Types of ROS, their formation sites in photosynthetic cells, and the damage they cause to the cellular components are described at the beginning. Furthermore, heavy metals are characterized in more detail, including their chemical properties, roles they play in living cells, sources of contamination, biochemical mechanisms of toxicity, and stress symptoms. The following subchapters contain the description of low-molecular-weight antioxidants and ROS-detoxifying enzymes, their properties, cellular localization, and the occurrence in algae belonging to different clades, as well as the summary of the results of the experiments concerning antioxidant response in heavy metal-treated eukaryotic algae. Other mechanisms providing tolerance to metal ions are briefly outlined at the end.

Keywords: Antioxidant enzymes; Eukaryotic algae; Heavy metals; Low-molecular-weight antioxidants; Oxidative stress; Toxicity mechanisms.

Fig. 1

Major mechanisms of toxicity of certain heavy metals

Fig. 2

Reactive oxygen species, their inter-conversions, and reactions with lipids (a) and with ions of redox-active metals (b). ROS and lipid radicals formed during lipid peroxidation are marked in black bold font. Empty arrows indicate both non-enzymatic and enzyme-catalysed reactions. E, excitation energy; L, lipid

Fig. 3

Major hydrophilic and hydrophobic low-molecular-weight antioxidants occurring in photosynthetic organisms and the ability of these compounds to detoxify ROS and organic radicals. Thick arrows symbolize participation in non-enzymatic (NR) or enzymatic (ER) regeneration of other antioxidants. Narrow arrow symbolizes enzymatic reduction of PQ to PQH₂. Cellular localization of particular compounds and enzymes was described in the text. All the compounds shown react with OH^•. APX, ascorbate peroxidase; Asc, ascorbate; Car, carotenoids; GPX, glutathione peroxidase; GR, glutathione reductase; GRX, glutaredoxin; GSH, glutathione; Org Rad, organic radicals; Phe, phenolic compounds; POX, peroxidase using phenolic compound as a reductant; PQ, plastoquinone; PQH₂, plastoquinol; Pro, proline; Toc, tocopherol

Fig. 4

Major reactive oxygen species-detoxifying enzymes and recycling of their cofactors (a), thioredoxin-peroxiredoxin-glutaredoxin system (b), and the versatility of reactions catalysed by various glutathione peroxidases (c). Enzyme cofactors are marked by grey font. Grey arrows are used to show reduction of peroxides or oxidized thiol groups of proteins. APX, ascorbate peroxidase; Asc, ascorbate; CAT, catalase; DHA, dehydroascorbate; DHAR, dehydroascorbate reductase; Fd_red, reduced ferredoxin, Fd_ox, oxidized ferredoxin; GPX, glutathione peroxidase; GR, glutathione reductase; GRX, glutaredoxin; GSH, glutathione; GSSG, glutathione disulphide; MDHA, monodehydroascorbate; MDHAR, monodehydroascorbate reductase; PRX, peroxiredoxin; SOD, superoxide dismutase; TRX, thioredoxin; TR, thioredoxin reductase

Fig. 5

Major mechanisms of heavy metal detoxification in algae. In some species, heavy metal ions are sequestered not in the vacuole, but in plastids or mitochondria