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Pressure accelerates the circadian clock of cyanobacteria

Although organisms are exposed to various pressure and temperature conditions, information remains limited on how pressure affects biological rhythms. This study investigated how hydrostatic pressure affects the circadian clock (KaiA, KaiB, and KaiC) of cyanobacteria. While the circadian rhythm is i...

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Autores principales: Kitahara, Ryo, Oyama, Katsuaki, Kawamura, Takahiro, Mitsuhashi, Keita, Kitazawa, Soichiro, Yasunaga, Kazuhiro, Sagara, Natsuno, Fujimoto, Megumi, Terauchi, Kazuki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6712028/
https://www.ncbi.nlm.nih.gov/pubmed/31455816
http://dx.doi.org/10.1038/s41598-019-48693-1
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author Kitahara, Ryo
Oyama, Katsuaki
Kawamura, Takahiro
Mitsuhashi, Keita
Kitazawa, Soichiro
Yasunaga, Kazuhiro
Sagara, Natsuno
Fujimoto, Megumi
Terauchi, Kazuki
author_facet Kitahara, Ryo
Oyama, Katsuaki
Kawamura, Takahiro
Mitsuhashi, Keita
Kitazawa, Soichiro
Yasunaga, Kazuhiro
Sagara, Natsuno
Fujimoto, Megumi
Terauchi, Kazuki
author_sort Kitahara, Ryo
collection PubMed
description Although organisms are exposed to various pressure and temperature conditions, information remains limited on how pressure affects biological rhythms. This study investigated how hydrostatic pressure affects the circadian clock (KaiA, KaiB, and KaiC) of cyanobacteria. While the circadian rhythm is inherently robust to temperature change, KaiC phosphorylation cycles that were accelerated from 22 h at 1 bar to 14 h at 200 bars caused the circadian-period length to decline. This decline was caused by the pressure-induced enhancement of KaiC ATPase activity and allosteric effects. Because ATPase activity was elevated in the CI and CII domains of KaiC, while ATP hydrolysis had negative activation volumes (ΔV(≠)), both domains played key roles in determining the period length of the KaiC phosphorylation cycle. The thermodynamic contraction of the structure of the active site during the transition state might have positioned catalytic residues and lytic water molecules favourably to facilitate ATP hydrolysis. Internal cavities might represent sources of compaction and structural rearrangement in the active site. Overall, the data indicate that pressure differences could alter the circadian rhythms of diverse organisms with evolved thermotolerance, as long as enzymatic reactions defining period length have a specific activation volume.
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spelling pubmed-67120282019-09-13 Pressure accelerates the circadian clock of cyanobacteria Kitahara, Ryo Oyama, Katsuaki Kawamura, Takahiro Mitsuhashi, Keita Kitazawa, Soichiro Yasunaga, Kazuhiro Sagara, Natsuno Fujimoto, Megumi Terauchi, Kazuki Sci Rep Article Although organisms are exposed to various pressure and temperature conditions, information remains limited on how pressure affects biological rhythms. This study investigated how hydrostatic pressure affects the circadian clock (KaiA, KaiB, and KaiC) of cyanobacteria. While the circadian rhythm is inherently robust to temperature change, KaiC phosphorylation cycles that were accelerated from 22 h at 1 bar to 14 h at 200 bars caused the circadian-period length to decline. This decline was caused by the pressure-induced enhancement of KaiC ATPase activity and allosteric effects. Because ATPase activity was elevated in the CI and CII domains of KaiC, while ATP hydrolysis had negative activation volumes (ΔV(≠)), both domains played key roles in determining the period length of the KaiC phosphorylation cycle. The thermodynamic contraction of the structure of the active site during the transition state might have positioned catalytic residues and lytic water molecules favourably to facilitate ATP hydrolysis. Internal cavities might represent sources of compaction and structural rearrangement in the active site. Overall, the data indicate that pressure differences could alter the circadian rhythms of diverse organisms with evolved thermotolerance, as long as enzymatic reactions defining period length have a specific activation volume. Nature Publishing Group UK 2019-08-27 /pmc/articles/PMC6712028/ /pubmed/31455816 http://dx.doi.org/10.1038/s41598-019-48693-1 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Kitahara, Ryo
Oyama, Katsuaki
Kawamura, Takahiro
Mitsuhashi, Keita
Kitazawa, Soichiro
Yasunaga, Kazuhiro
Sagara, Natsuno
Fujimoto, Megumi
Terauchi, Kazuki
Pressure accelerates the circadian clock of cyanobacteria
title Pressure accelerates the circadian clock of cyanobacteria
title_full Pressure accelerates the circadian clock of cyanobacteria
title_fullStr Pressure accelerates the circadian clock of cyanobacteria
title_full_unstemmed Pressure accelerates the circadian clock of cyanobacteria
title_short Pressure accelerates the circadian clock of cyanobacteria
title_sort pressure accelerates the circadian clock of cyanobacteria
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6712028/
https://www.ncbi.nlm.nih.gov/pubmed/31455816
http://dx.doi.org/10.1038/s41598-019-48693-1
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