Copper is an essential micronutrient, but at supraoptimal concentrations it is also highly toxic, inducing oxidative stress and disrupting photosynthesis. The aim of the present study was to analyze selected protective mechanisms in strains ofChlamydomonas reinhardtiiadapted and not adapted for growth in the presence of elevated copper concentrations. Two algal lines (tolerant and non-tolerant to high Cu2+concentrations) were used in experiments to study photosynthetic pigment content, peroxidase activity, and non-photochemical quenching. The content of prenyllipids was studied in four different algal lines (two of the same as above and two new ones). The copper-adapted strains contained about 2.6 times more α-tocopherol and plastoquinol and about 1.7 times more total plastoquinone than non-tolerant strains. Exposure to excess copper led to oxidation of the plastoquinone pool in non-tolerant strains, whereas this effect was less pronounced or did not occur in copper-tolerant strains. Peroxidase activity was approximately 1.75 times higher in the tolerant strain than in the non-tolerant one. The increase in peroxidase activity in the tolerant strain was less pronounced when the algae were grown in dim light. In the tolerant line nonphotochemical quenching was induced faster and was usually about 20–30% more efficient than in the non-tolerant line. The improvement of antioxidant defense and photoprotection may be important factors in the evolutionary processes leading to tolerance to heavy metals.