Shimakawa 2020 Int J Mol Sci

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Shimakawa G, Kohara A, Miyake C (2020) Characterization of light-enhanced respiration in cyanobacteria. Int J Mol Sci 22:342. doi: 10.3390/ijms22010342.

» PMID: 33396191 Open Access

Shimakawa G, Kohara A, Miyake C (2020) Int J Mol Sci

Abstract: In eukaryotic algae, respiratory O2 uptake is enhanced after illumination, which is called light-enhanced respiration (LER). It is likely stimulated by an increase in respiratory substrates produced during photosynthetic CO2 assimilation and function in keeping the metabolic and redox homeostasis in the light in eukaryotic cells, based on the interactions among the cytosol, chloroplasts, and mitochondria. Here, we first characterize LER in photosynthetic prokaryote cyanobacteria, in which respiration and photosynthesis share their metabolisms and electron transport chains in one cell. From the physiological analysis, the cyanobacterium Synechocystis sp. PCC 6803 performs LER, similar to eukaryotic algae, which shows a capacity comparable to the net photosynthetic O2 evolution rate. Although the respiratory and photosynthetic electron transports share the interchain, LER was uncoupled from photosynthetic electron transport. Mutant analyses demonstrated that LER is motivated by the substrates directly provided by photosynthetic CO2 assimilation, but not by glycogen. Further, the light-dependent activation of LER was observed even with exogenously added glucose, implying a regulatory mechanism for LER in addition to the substrate amounts. Finally, we discuss the physiological significance of the large capacity of LER in cyanobacteria and eukaryotic algae compared to those in plants that normally show less LER.

Bioblast editor: Gnaiger E

Selected quotes

  • In a variety of eukaryotic algae, the O2 uptake rate during dark respiration is frequently higher after illumination and can then reach about half of the photosynthetic O2 evolution rate. The light-enhanced dark respiration (here we termed it as light-enhanced respiration, LER), one of the most indisputable phenomena that shows respiration is linked to photosynthesis under light conditions, is associated with the amounts of respiratory substrates generated during photosynthesis in eukaryotic algae [4,13–16]. However, the details of the initiation and relaxation mechanism of LER are still unclear.
  • The interaction between respiration and photosynthesis has already been established in cyanobacteria, the prokaryotic algae broadly recognized as the progenitor of oxygenic photosynthesis [17–19]. Due to the lack of organelles, both respiration and photosynthesis proceed in one cell, and they both depend on the cytosolic metabolism and on the electron transport chain in the thylakoid membrane.
  • After the actinic light was switched off, the O2 uptake rate was approximately 40 µmol O2 mg Chl−1 h−1, which was designated as LER in this study. The LER was relieved within 20 min, and finally, the O2 uptake rate was close to 10 µmol O2 mg Chl−1 h−1 (Figure 2 and Figure S1), which was consistent with the values previously detected in the S. 6803 wild type [21].
  • Contrary to the decrease in net photosynthetic O2 evolution rate, a increase in LER was observed with the time of illumination (Figure 3A). If any O2-dependent alternative electron transports do not compete with the CO2 assimilation in this situation, the sum of net O2 evolution and LER rates can be defined as the total photosynthetic O2 evolution rate corresponding to the gross photosynthetic activity. The total photosynthetic O2 evolution rate was kept almost constant and correlated with the effective quantum yield of PSII, Y(II), during illumination (Figure 3B). Overall, the decrease in the net O2 evolution rate reflected the increase in LER but not an inactivation of CO2 assimilation.
  • The proportional relationship between LER and the total photosynthetic O2 evolution rate indicates that LER is activated, paralleled with the photosynthetic CO2 assimilation.
  • In all plants, except the C4 plants, postillumination transient O2 uptake is largely observed at a CO2 compensation point and is driven by photorespiration [40,41].
  • Overall, these mutant analyses suggested that O2-dependent alternative electron transport such as FLV-mediated Mehler-like reactions and photorespiration are not included in the LER.
  • The large amount of O2 consumed after an actinic light is turned off corresponds to the amount of substrate for respiration or photorespiration produced in the light [41]. Therefore, the analysis of postillumination transient O2 uptake is a useful method to uncover the molecular mechanism of O2-consuming reactions during photosynthesis.
  • It is assumed that the physiological significance of LER is the immediate production of ATP using excess photosynthates. In other words, ATP is additionally demanded even during photosynthesis, probably for a variety of cell metabolisms.

Cited by

  • Went N, Di Marcello M, Gnaiger E (2021) Oxygen dependence of photosynthesis and light-enhanced dark respiration studied by High-Resolution PhotoRespirometry. MitoFit Prep 2021.5. - »Bioblast link«

Labels: MiParea: Respiration 

Organism: Eubacteria 

Preparation: Intact cells 

Coupling state: ROUTINE 

Algae, LEDR, Photosynthesis, MitoFit 2021.5 PB