Activation of oxidative carbon metabolism by nutritional enrichment by photosynthesis and exogenous organic compounds in the red alga Cyanidioschyzon merolae: evidence for heterotrophic growth

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.