“Safe” cellular proliferation depending on “toxic” photosynthesis

Day/Night Separation of Oxygenic Energy Metabolism and Nuclear DNA Replication in the Unicellular Red Alga Cyanidioschyzon merolae.

Shin-ya Miyagishima, Atsuko Era, Tomohisa Hasunuma, Mami Matsuda, Shunsuke Hirooka, Nobuko Sumiya, Akihiko Kondo, Takayuki Fujiwara

mBio 10(4), e00833-19, 2019 DOI:10.1128/mBio.00833-19

Eukaryotes acquired chloroplasts through an endosymbiotic event in which a cyanobacterium or a unicellular eukaryotic alga was integrated into a previously nonphotosynthetic eukaryotic cell. Photosynthesis by chloroplasts enabled algae to expand their habitats and led to further evolution of land plants. However, photosynthesis causes greater oxidative stress than mitochondrion-based respiration. In seed plants, cell division is restricted to nonphotosynthetic meristematic tissues and populations of photosynthetic cells expand without cell division. Thus, seemingly, photosynthesis is spatially sequestrated from cell proliferation. In contrast, eukaryotic algae possess photosynthetic chloroplasts throughout their life cycle. Here we show that oxygenic energy conversion (daytime) and nuclear DNA replication (night time) are temporally sequestrated in C. merolae. This sequestration enables “safe” proliferation of cells and allows coexistence of chloroplasts and the eukaryotic host cell, as shown in yeast, where mitochondrial respiration and nuclear DNA replication are temporally sequestrated to reduce the mutation rate.

Figure1

Figure1: The unicellular red alga Cyanidioschyzon merolae was cultured under a 12-h light / 12-h dark cycle. The cells early in the dark period (dark) were illuminated (light) either with or without DCMU (photosynthetic inhibitor) or TEMPOL (ROS scavenger). The green fluorescence indicates accumulation of MRE11 in the nucleus (DNA double strand break). The red is autofluorescence of the chloroplast. When the cells during the subjective night perform photosynthesis, the frequency of nuclear DSB (arrowheads) increases.

Figure1

Figure2: The temporal separation of ROS-generating oxygenic energy metabolism by mitochondria and chloroplasts (endosymbiotic organelles) and nuclear DNA replication (eukaryotic host cell) ensures safe cell proliferation


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