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Day/Night Separation of Oxygenic Energy Metabolism and Nuclear DNA Replication in the Unicellular Red Alga Cyanidioschyzon merolae

The transition from G(1) to S phase and subsequent nuclear DNA replication in the cells of many species of eukaryotic algae occur predominantly during the evening and night in the absence of photosynthesis; however, little is known about how day/night changes in energy metabolism and cell cycle prog...

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Autores principales: Miyagishima, Shin-ya, Era, Atsuko, Hasunuma, Tomohisa, Matsuda, Mami, Hirooka, Shunsuke, Sumiya, Nobuko, Kondo, Akihiko, Fujiwara, Takayuki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6606799/
https://www.ncbi.nlm.nih.gov/pubmed/31266864
http://dx.doi.org/10.1128/mBio.00833-19
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author Miyagishima, Shin-ya
Era, Atsuko
Hasunuma, Tomohisa
Matsuda, Mami
Hirooka, Shunsuke
Sumiya, Nobuko
Kondo, Akihiko
Fujiwara, Takayuki
author_facet Miyagishima, Shin-ya
Era, Atsuko
Hasunuma, Tomohisa
Matsuda, Mami
Hirooka, Shunsuke
Sumiya, Nobuko
Kondo, Akihiko
Fujiwara, Takayuki
author_sort Miyagishima, Shin-ya
collection PubMed
description The transition from G(1) to S phase and subsequent nuclear DNA replication in the cells of many species of eukaryotic algae occur predominantly during the evening and night in the absence of photosynthesis; however, little is known about how day/night changes in energy metabolism and cell cycle progression are coordinated and about the advantage conferred by the restriction of S phase to the night. Using a synchronous culture of the unicellular red alga Cyanidioschyzon merolae, we found that the levels of photosynthetic and respiratory activities peak during the morning and then decrease toward the evening and night, whereas the pathways for anaerobic consumption of pyruvate, produced by glycolysis, are upregulated during the evening and night as reported recently in the green alga Chlamydomonas reinhardtii. Inhibition of photosynthesis by 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) largely reduced respiratory activity and the amplitude of the day/night rhythm of respiration, suggesting that the respiratory rhythm depends largely on photosynthetic activity. Even when the timing of G(1)/S-phase transition was uncoupled from the day/night rhythm by depletion of retinoblastoma-related (RBR) protein, the same patterns of photosynthesis and respiration were observed, suggesting that cell cycle progression and energy metabolism are regulated independently. Progression of the S phase under conditions of photosynthesis elevated the frequency of nuclear DNA double-strand breaks (DSB). These results suggest that the temporal separation of oxygenic energy metabolism, which causes oxidative stress, from nuclear DNA replication reduces the risk of DSB during cell proliferation in C. merolae.
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spelling pubmed-66067992019-07-08 Day/Night Separation of Oxygenic Energy Metabolism and Nuclear DNA Replication in the Unicellular Red Alga Cyanidioschyzon merolae Miyagishima, Shin-ya Era, Atsuko Hasunuma, Tomohisa Matsuda, Mami Hirooka, Shunsuke Sumiya, Nobuko Kondo, Akihiko Fujiwara, Takayuki mBio Research Article The transition from G(1) to S phase and subsequent nuclear DNA replication in the cells of many species of eukaryotic algae occur predominantly during the evening and night in the absence of photosynthesis; however, little is known about how day/night changes in energy metabolism and cell cycle progression are coordinated and about the advantage conferred by the restriction of S phase to the night. Using a synchronous culture of the unicellular red alga Cyanidioschyzon merolae, we found that the levels of photosynthetic and respiratory activities peak during the morning and then decrease toward the evening and night, whereas the pathways for anaerobic consumption of pyruvate, produced by glycolysis, are upregulated during the evening and night as reported recently in the green alga Chlamydomonas reinhardtii. Inhibition of photosynthesis by 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) largely reduced respiratory activity and the amplitude of the day/night rhythm of respiration, suggesting that the respiratory rhythm depends largely on photosynthetic activity. Even when the timing of G(1)/S-phase transition was uncoupled from the day/night rhythm by depletion of retinoblastoma-related (RBR) protein, the same patterns of photosynthesis and respiration were observed, suggesting that cell cycle progression and energy metabolism are regulated independently. Progression of the S phase under conditions of photosynthesis elevated the frequency of nuclear DNA double-strand breaks (DSB). These results suggest that the temporal separation of oxygenic energy metabolism, which causes oxidative stress, from nuclear DNA replication reduces the risk of DSB during cell proliferation in C. merolae. American Society for Microbiology 2019-07-02 /pmc/articles/PMC6606799/ /pubmed/31266864 http://dx.doi.org/10.1128/mBio.00833-19 Text en Copyright © 2019 Miyagishima et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Miyagishima, Shin-ya
Era, Atsuko
Hasunuma, Tomohisa
Matsuda, Mami
Hirooka, Shunsuke
Sumiya, Nobuko
Kondo, Akihiko
Fujiwara, Takayuki
Day/Night Separation of Oxygenic Energy Metabolism and Nuclear DNA Replication in the Unicellular Red Alga Cyanidioschyzon merolae
title Day/Night Separation of Oxygenic Energy Metabolism and Nuclear DNA Replication in the Unicellular Red Alga Cyanidioschyzon merolae
title_full Day/Night Separation of Oxygenic Energy Metabolism and Nuclear DNA Replication in the Unicellular Red Alga Cyanidioschyzon merolae
title_fullStr Day/Night Separation of Oxygenic Energy Metabolism and Nuclear DNA Replication in the Unicellular Red Alga Cyanidioschyzon merolae
title_full_unstemmed Day/Night Separation of Oxygenic Energy Metabolism and Nuclear DNA Replication in the Unicellular Red Alga Cyanidioschyzon merolae
title_short Day/Night Separation of Oxygenic Energy Metabolism and Nuclear DNA Replication in the Unicellular Red Alga Cyanidioschyzon merolae
title_sort day/night separation of oxygenic energy metabolism and nuclear dna replication in the unicellular red alga cyanidioschyzon merolae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6606799/
https://www.ncbi.nlm.nih.gov/pubmed/31266864
http://dx.doi.org/10.1128/mBio.00833-19
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