Cargando…
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...
Autores principales: | , , , , , , , |
---|---|
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 |
_version_ | 1783431971743989760 |
---|---|
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. |
format | Online Article Text |
id | pubmed-6606799 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT miyagishimashinya daynightseparationofoxygenicenergymetabolismandnucleardnareplicationintheunicellularredalgacyanidioschyzonmerolae AT eraatsuko daynightseparationofoxygenicenergymetabolismandnucleardnareplicationintheunicellularredalgacyanidioschyzonmerolae AT hasunumatomohisa daynightseparationofoxygenicenergymetabolismandnucleardnareplicationintheunicellularredalgacyanidioschyzonmerolae AT matsudamami daynightseparationofoxygenicenergymetabolismandnucleardnareplicationintheunicellularredalgacyanidioschyzonmerolae AT hirookashunsuke daynightseparationofoxygenicenergymetabolismandnucleardnareplicationintheunicellularredalgacyanidioschyzonmerolae AT sumiyanobuko daynightseparationofoxygenicenergymetabolismandnucleardnareplicationintheunicellularredalgacyanidioschyzonmerolae AT kondoakihiko daynightseparationofoxygenicenergymetabolismandnucleardnareplicationintheunicellularredalgacyanidioschyzonmerolae AT fujiwaratakayuki daynightseparationofoxygenicenergymetabolismandnucleardnareplicationintheunicellularredalgacyanidioschyzonmerolae |