Day/night separation of oxygenic energy metabolism and nuclear DNA replication in the unicellular red alga Cyanidioschyzon merolae
Day/night separation of oxygenic energy metabolism and nuclear DNA replication in the unicellular red alga Cyanidioschyzon merolae
复制标题
单细胞红藻 Cyanidioschyzon merolae 中氧能代谢和核 DNA 复制的昼夜分离
作者：
Miyagishima;S.;Era;A.;Hasunuma;T.;Matsuda;M.;Hirooka;S.;Sumiya;N.;Kondo;A.;Fujiwara;T.
从G1期到S期的过渡和随后的核DNA复制在许多真核藻类的细胞中主要发生在晚上和夜间，在没有光合作用的情况下，然而，很少有人知道白天/夜间的能量代谢和细胞周期进程的变化是如何协调的，以及关于限制S期到夜间所带来的优势。使用同步培养的单细胞Cyanidioschyzon merolae，我们发现，光合和呼吸活动的水平在早上达到峰值，然后减少到傍晚和夜间，而无氧消耗的丙酮酸，糖酵解产生的途径，上调在傍晚和夜间最近报道的绿色衣藻莱茵衣藻。3-（3，4-二氯苯基）-1，1-二甲基脲（DCMU）对光合作用的抑制作用大大降低了呼吸活动和呼吸昼夜节律的幅度，表明呼吸节律在很大程度上取决于光合作用活性。即使当G1/S-相转变的时间是从白天/黑夜节奏的视网膜母细胞瘤相关（RBR）蛋白耗尽解耦，观察到相同的模式的光合作用和呼吸，这表明细胞周期的进展和能量代谢的调节独立。在光合作用条件下，S期的进展提高了核DNA双链断裂（DSB）的频率。这些结果表明，导致氧化应激的氧能代谢与核DNA复制的时间分离降低了C.重要意义真核生物通过内共生事件获得叶绿体，其中蓝细菌或单细胞真核生物整合到先前非光合作用的真核细胞中。叶绿体的光合作用使藻类能够扩大它们的栖息地，并导致陆地植物的进一步进化。然而，光合作用比基于光合作用的呼吸作用引起更大的氧化应激。在种子植物中，细胞分裂仅限于非光合分生组织，光合细胞群体在没有细胞分裂的情况下扩大。因此，似乎光合作用在空间上与细胞增殖隔离。相反，真核藻类在其整个生命周期中都具有光合叶绿体。在这里，我们表明，含氧能量转换（白天）和核DNA复制（夜间）的时间封存在C。merolae。这种隔离使细胞能够“安全”增殖，并允许叶绿体和真核宿主细胞共存，如酵母中所示，其中线粒体呼吸和核DNA复制被暂时隔离以降低突变率。
The transition from G1to S phase and subsequent nuclear DNA replication in the cells of many species of eukaryotic algae occur predominantly during the evening and night in the absence of photosynthesis; however, little is known about how day/night changes in energy metabolism and cell cycle progression are coordinated and about the advantage conferred by the restriction of S phase to the night. Using a synchronous culture of the unicellular red alga Cyanidioschyzon merolae, we found that the levels of photosynthetic and respiratory activities peak during the morning and then decrease toward the evening and night, whereas the pathways for anaerobic consumption of pyruvate, produced by glycolysis, are upregulated during the evening and night as reported recently in the green alga Chlamydomonas reinhardtii. Inhibition of photosynthesis by 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) largely reduced respiratory activity and the amplitude of the day/night rhythm of respiration, suggesting that the respiratory rhythm depends largely on photosynthetic activity. Even when the timing of G1/S-phase transition was uncoupled from the day/night rhythm by depletion of retinoblastoma-related (RBR) protein, the same patterns of photosynthesis and respiration were observed, suggesting that cell cycle progression and energy metabolism are regulated independently. Progression of the S phase under conditions of photosynthesis elevated the frequency of nuclear DNA double-strand breaks (DSB). These results suggest that the temporal separation of oxygenic energy metabolism, which causes oxidative stress, from nuclear DNA replication reduces the risk of DSB during cell proliferation in C. merolae.IMPORTANCEEukaryotes 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.