Abstract
Fluctuating light is the norm for photosynthetic organisms, with a wide range of frequencies (0.00001 to 10 Hz) owing to diurnal cycles, cloud cover, canopy shifting and mixing; with broad implications for climate change, agriculture and bioproduct production. Photosynthetic growth in fluctuating light is generally considered to improve with increasing fluctuation frequency. Here we demonstrate that the regulation of photosynthesis imposes a penalty on growth in fluctuating light for frequencies in the range of 0.01 to 0.1 Hz (organisms studied: Synechococcus elongatus and Chlamydomonas reinhardtii). We provide a comprehensive sweep of frequencies and duty cycles. In addition, we develop a 2nd order model that identifies the source of the penalty to be the regulation of the Calvin cycle – present at all frequencies but compensated at high frequencies by slow kinetics of RuBisCO.
Highlights
In nature, solar flux is discontinuous, fluctuating due to the diurnal cycle, varying cloud cover, canopy shifting and circulation in bodies of water, photosynthetic organisms are exposed to a diverse set of fluctuating light profiles ranging from 0.00001 to 10 Hz1–4
Synechococcus elongatus is frequently used in biotechnology since it can be transformed for chemical production or increased growth[40,41]
This work presents evidence that the regulation of photosynthesis in fluctuating light has an adverse effect on photoautotrophic growth, strong in a range around 0.01–0.1 Hz - a range that is typical of nature, agriculture, and industry
Summary
Solar flux is discontinuous, fluctuating due to the diurnal cycle, varying cloud cover, canopy shifting and circulation in bodies of water, photosynthetic organisms are exposed to a diverse set of fluctuating light profiles ranging from 0.00001 to 10 Hz1–4. The light independent reactions use the products from the light dependent reaction (ATP and NADPH) to reduce carbon via the Calvin cycle. High frequency fluctuations allow for continuous growth through a mismatch of reaction rates, rapid light harvesting reactions and slower enzymatic reactions[13,18,19]. The mismatch is between (i) the rapid light-driven generation of ATP and NADPH by the photosynthetic electron transport chain and (ii) the slower Calvin cycle[13,18,19,27]. Case of very high frequencies, (>100 Hz), mismatches along the photosynthetic electron transport chain can contribute to the flashing light effect[14,28,29]
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