Dark accumulation of downstream glycolytic intermediates initiates robust photosynthesis in cyanobacteria

Dark accumulation of downstream glycolytic intermediates initiates robust photosynthesis in cyanobacteria
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DOI:
10.1093/plphys/kiac602
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发表时间:
2022-12-27
期刊:
影响因子:
7.4
通讯作者:
Hasunuma,Tomohisa
Hasunuma,Tomohisa
中科院分区:
生物学1区
文献类型:
--
作者:
Tanaka,Kenya;Shirai,Tomokazu;Hasunuma,Tomohisa

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Photosynthesis must maintain stability and robustness throughout fluctuating natural environments. In cyanobacteria, dark-to-light transition leads to drastic metabolic changes from dark respiratory metabolism to CO2fixation through the Calvin–Benson–Bassham (CBB) cycle using energy and redox equivalents provided by photosynthetic electron transfer. Previous studies have shown that catabolic metabolism supports the smooth transition into CBB cycle metabolism. However, metabolic mechanisms for robust initiation of photosynthesis are poorly understood due to lack of dynamic metabolic characterizations of dark-to-light transitions. Here, we show rapid dynamic changes (on a time scale of seconds) in absolute metabolite concentrations and13C tracer incorporation after strong or weak light irradiation in the cyanobacteriumSynechocystissp. PCC 6803. Integration of this data enabled estimation of time-resolved nonstationary metabolic flux underlying CBB cycle activation. This dynamic metabolic analysis indicated that downstream glycolytic intermediates, including phosphoglycerate and phosphoenolpyruvate, accumulate under dark conditions as major substrates for initial CO2fixation. Compared with wild-typeSynechocystis, significant decreases in the initial oxygen evolution rate were observed in 12 h dark preincubated mutants deficient in glycogen degradation or oxidative pentose phosphate pathways. Accordingly, the degree of decrease in the initial oxygen evolution rate was proportional to the accumulated pool size of glycolytic intermediates. These observations indicate that the accumulation of glycolytic intermediates is essential for efficient metabolism switching under fluctuating light environments.