Selective loss of photosystem I and formation of tubular thylakoids in heterotrophically grown red alga Cyanidioschyzon merolae

  • Takashi Moriyama
  • Natsumi Mori
  • Noriko Nagata
  • Naoki SatoEmail author
Original Article


We previously found that glycerol is required for heterotrophic growth in the unicellular red alga Cyanidioschyzon merolae. Here, we analyzed heterotrophically grown cells in more detail. Sugars or other organic substances did not support the growth in the dark. The growth rate was 0.4 divisions day−1 in the presence of 400 mM glycerol, in contrast with 0.5 divisions day−1 in the phototrophic growth. The growth continued until the sixth division. Unlimited heterotrophic growth was possible in the medium containing DCMU and glycerol in the light. Light-activated heterotrophic culture in which cells were irradiated by intermittent light also continued without an apparent limit. In the heterotrophic culture in the dark, chlorophyll content drastically decreased, as a result of inability of dark chlorophyll synthesis. Photosynthetic activity gradually decreased over 10 days, and finally lost after 19 days. Low-temperature fluorescence measurement and immunoblot analysis showed that this decline in photosynthetic activity was mainly due to the loss of Photosystem I, while the levels of Photosystem II and phycobilisomes were maintained. Accumulated triacylglycerol was lost during the heterotrophic growth, while keeping the overall lipid composition. Observation by transmission electron microscopy revealed that a part of thylakoid membranes turned into pentagonal tubular structures, on which five rows of phycobilisomes were aligned. This might be a structure that compactly conserve phycobilisomes and Photosystem II in an inactive state, probably as a stock of carbon and nitrogen. These results suggest that C. merolae has a unique strategy of heterotrophic growth, distinct from those found in other red algae.


Glycerol nutrition Heterotrophic growth Red alga Tubular thylakoid 



We thank Ms. Megumi Kobayashi, Japan Women’s University, for technical assistance in tomography, Dr. Koichi Kobayashi, Osaka Prefectural University, for technical advice in measurement of low-temperature fluorescence, and Prof. Hajime Wada, University of Tokyo, for discussion on fluorescence measurement.

Author Contributions

TM and NM performed all experiments; NN performed tomography; NS conceived the research and performed electron microscopy.


This work was supported in part by Core Research for Evolutional Science and Technology (CREST) from the Japan Science and Technology Agency (JST) and a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan (Grant. No. 17H03715).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The manuscript has not been submitted elsewhere to other journals for simultaneous consideration. It is an expansion of our previous works, but no materials were re-used. No data have been fabricated or manipulated. No data, text, or theories by others are presented as if they were the author’s own.

Human and animal participants

This research does not involve human participants or animals.

Informed consent

This research does not require informed consent. Consent to submit has been received explicitly from all co-authors.

Supplementary material

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Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Life Sciences, Graduate School of Arts and SciencesThe University of TokyoTokyoJapan
  2. 2.Department of Chemical Biological Sciences, Faculty of ScienceJapan Women’s UniversityTokyoJapan

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