Chlorella vulgaris integrates photoperiod and chloroplast redox signals in response to growth at high light

Main conclusionPhotoacclimation to variable light and photoperiod regimes in C. vulgaris represents a complex interplay between biogenic phytochrome-mediated sensing and operational redox sensing signaling pathways.Chlorella vulgaris Beijerinck UTEX 265 exhibits a yellow-green phenotype when grown under high light (HL) in contrast to a dark green phenotype when grown at low light (LL). The redox state of the photosynthetic electron transport chain (PETC) as estimated by excitation pressure has been proposed to govern this phenotypic response. We hypothesized that if the redox state of the PETC was the sole regulator of the HL phenotype, C. vulgaris should photoacclimate in response to the steady-state excitation pressure during the light period regardless of the length of the photoperiod. As expected, LL-grown cells exhibited a dark green phenotype, low excitation pressure (1-qP=0.22 +/- 0.02), high chlorophyll (Chl) content (375 +/- 77fg Chl/cell), low Chl a/b ratio (2.97 +/- 0.18) as well as high photosynthetic efficiency and photosynthetic capacity regardless of the photoperiod. In contrast, C. vulgaris grown under continuous HL developed a yellow-green phenotype characterized by high excitation pressure (1-qP=0.68 +/- 0.01), a relatively low Chl content (180 +/- 53fg Chl/cell), high Chl a/b ratio (6.36 +/- 0.54) with concomitantly reduced light-harvesting polypeptide abundance, as well as low photosynthetic capacity and efficiency measured on a per cell basis. Although cells grown under HL and an 18h photoperiod developed a typical yellow-green phenotype, cells grown at HL but a 12h photoperiod exhibited a dark green phenotype comparable to LL-grown cells despite exhibiting growth under high excitation pressure (1-qP=0.80 +/- 0.04). The apparent uncoupling of excitation pressure and phenotype in HL-grown cells and a 12h photoperiod indicates that chloroplast redox status cannot be the sole regulator of photoacclimation in C. vulgaris. We conclude that photoacclimation in C. vulgaris to HL is dependent upon growth history and reflects a complex interaction of endogenous systems that sense changes in photoperiod as well as photosynthetic redox balance.