Non-photochemical quenching in the cells of the carotenogenic chlorophyte Haematococcus lacustris under favorable conditions and under stress

The microalga Haematococcus lacustris (formerly H. pluvialis) is the richest source of the valuable pigment astaxanthin, accumulated in red aplanospores (haematocysts). In this work, we report on the photoprotective mechanisms in H. lacustris, conveying this microalga its ability to cope with a wide range of adverse conditions, with special emphasis put on non-photochemical quenching (NPQ) of the excited chlorophyll states. We studied the changes in the primary photochemistry of the photosystems (PS) as a function of irradiance and the physiological state. We leveraged the transcriptomic data to gain a deeper insight into possible NPQ mechanisms in this microalga. Peculiar to H. lacustris is a bi-phasic pattern of changes in photoprotection during haematocyst formation. The first phase coincides with a transient rise of photosynthetic activity. Based on transcriptomic data, high NPQ level in the first phase is maintained predominantly by the expression of PsbS and LhcsR proteins. Then, (in mature haematocysts), stress tolerance is achieved by optical shielding by astaxanthin and dramatic reduction of photosynthetic apparatus. In contrast to many microalgae, shielding plays an important role in H. lacistris haematocysts, whereas regulated NPQ is suppressed. Astaxanthin is decoupled from the PS, hence the light energy is not transferred to reaction centers and dissipates as heat. It allows to retain a higher photochemical yield in haematocysts comparing to vegetative cells. The ability of H. lacustris to substitute the “classical” active photoprotective mechanisms such as NPQ with optic shielding and general metabolism quiescence makes this organism a useful model to reveal photoprotection mechanisms.