Abstract
Respiration is an important process in photosynthetic organisms, as it is in other organisms, for the supply of ATP and metabolites required for biosynthesis. Furthermore, individual enzymatic activity is subject to regulation by metabolic intermediates in glycolysis and the citric acid cycle. However, little is known about how glycolysis or catabolism are related to photosynthetic activity or accumulation of photosynthetic products. We previously developed a flat-plate culture apparatus assembled from materials commonly used for gel electrophoresis, which enables high-density culture of the unicellular red alga Cyanidioschyzon merolae. In this study, a stationary dense culture of C. merolae, when re-activated in this culture apparatus, exhibited an accumulation of photosynthetically produced starch. We demonstrated that respiratory activity increased during the culture period, while photosynthetic activity remained constant. Gene expression analysis revealed that the genes involved in cytosolic glycolysis and the citric acid cycle were selectively activated, compared to the genes for the oxidative pentose phosphate pathway and the Calvin–Benson cycle. Measurements of the respiratory rate after addition of various organic substances showed that C. merolae can utilize almost any exogenous organic compound as a respiratory substrate, although the effectiveness of each compound was dependent on the culture time in the flat-plate culture, suggesting that glycolysis was rate-limiting to respiration, and its activity depended on the level of photosynthetic products within the cells. We also demonstrated that organic substances increased the rate of cell growth under dim light and, interestingly, C. merolae could grow heterotrophically in the presence of glycerol. Obligate photoautotrophy should be considered an ecological, rather than physiological, characteristic of C. merolae.Electronic supplementary materialThe online version of this article (doi:10.1186/s40064-015-1365-0) contains supplementary material, which is available to authorized users.
Highlights
Photosynthetic organisms consume oxygen through respiration and produce it through photosynthetic oxygen evolution
Our results indicate that C. merolae efficiently utilizes various exogenous substrates for respiration and growth, and C. merolae can heterotrophically grow in glycerol-containing medium, but not in medium containing glucose, succinic acid, or lactic acid
Physiological changes in C. merolae cells grown in flat‐plate culture Previously, we reported a culture method using a flat-plate culture apparatus (Fig. 1a), which alleviates the restriction of light availability caused by the self-shading of cells in a culture of high cell density (Moriyama et al 2014b)
Summary
Photosynthetic organisms consume oxygen through respiration and produce it through photosynthetic oxygen evolution. The respiratory rate is estimated to be 1/6. Defects in a gene that encodes part of the respiratory chain lead to poor leaf growth and a decrease in the rate of photosynthesis (Vedel et al 1999). Plant respiration is regulated by phosphoenolpyruvate (PEP)-induced inhibition of ATP-dependent phosphofructokinase (PFK) and inverse activation of PFK by inorganic phosphate (Plaxton 1996). An increase in NADH concentration represses the activity of dehydrogenases in the citric acid cycle (McIntosh and Oliver 1992). In the green alga Chlorella pyrenoidosa, the rate of respiration is positively correlated with growth rate and gradually decreases in darkness (Geider and Osborne 1989). Regulation of the enzymatic reactions in glycolysis and the citric acid cycle has been observed, little is known about how respiratory activity relates to photosynthetic activity or to the accumulation of photosynthetic products
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