Initial nutrient condition determines the recovery speed of quiescent cells in fission yeast

Most of microbe cells spend the majority of their times in quiescence due to unfavorable environmental conditions. The study of this dominant state is crucial for understanding the basic cell physiology. Retained recovery ability is a critical property of quiescent cells, which consists of two featu...

Full description

Bibliographic Details
Main Authors: Qi Liu, Nan Sheng, Zhiwen Zhang, Chenjun He, Yao Zhao, Haoyuan Sun, Jianguo Chen, Xiaojing Yang, Chao Tang
Format: Article
Language:English
Published: Elsevier 2024-03-01
Series:Heliyon
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2405844024025891
_version_ 1797259885931397120
author Qi Liu
Nan Sheng
Zhiwen Zhang
Chenjun He
Yao Zhao
Haoyuan Sun
Jianguo Chen
Xiaojing Yang
Chao Tang
author_facet Qi Liu
Nan Sheng
Zhiwen Zhang
Chenjun He
Yao Zhao
Haoyuan Sun
Jianguo Chen
Xiaojing Yang
Chao Tang
author_sort Qi Liu
collection DOAJ
description Most of microbe cells spend the majority of their times in quiescence due to unfavorable environmental conditions. The study of this dominant state is crucial for understanding the basic cell physiology. Retained recovery ability is a critical property of quiescent cells, which consists of two features: how long the cells can survive (the survivability) and how fast they can recover (the recovery activity). While the survivability has been extensively studied under the background of chronological aging, how the recovery activity depends on the quiescent time and what factors influence its dynamics have not been addressed quantitatively. In this work, we systematically quantified both the survivability and the recovery activity of long-lived quiescent fission yeast cells at the single cell level under various nutrient conditions. It provides the most profound evolutionary dynamics of quiescent cell regeneration ability described to date. We found that the single cell recovery time linearly increased with the starvation time before the survivability significantly declined. This linearity was robust under various nutrient conditions and the recovery speed was predetermined by the initial nutrient condition. Transcriptome profiling further revealed that quiescence states under different nutrient conditions evolve in a common trajectory but with different speed. Our results demonstrated that cellular quiescence has a continuous spectrum of depths and its physiology is greatly influenced by environmental conditions.
first_indexed 2024-03-07T18:36:31Z
format Article
id doaj.art-bb0ac4df40e14b7d8a59224368cf9aca
institution Directory Open Access Journal
issn 2405-8440
language English
last_indexed 2024-04-24T23:16:33Z
publishDate 2024-03-01
publisher Elsevier
record_format Article
series Heliyon
spelling doaj.art-bb0ac4df40e14b7d8a59224368cf9aca2024-03-17T07:55:44ZengElsevierHeliyon2405-84402024-03-01105e26558Initial nutrient condition determines the recovery speed of quiescent cells in fission yeastQi Liu0Nan Sheng1Zhiwen Zhang2Chenjun He3Yao Zhao4Haoyuan Sun5Jianguo Chen6Xiaojing Yang7Chao Tang8Center for Quantitative Biology, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, China; The Key Laboratory of Cell Proliferation and Differentiation of Ministry of Education, School of Life Sciences, Peking University, Beijing, 100871, ChinaCenter for Quantitative Biology, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, ChinaPeking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, ChinaCollege of Life Science and Technology, Huazhong Agriculture University, Wuhan, 430070, ChinaCenter for Quantitative Biology, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, ChinaPeking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, ChinaCenter for Quantitative Biology, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, China; The Key Laboratory of Cell Proliferation and Differentiation of Ministry of Education, School of Life Sciences, Peking University, Beijing, 100871, ChinaCenter for Quantitative Biology, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, China; Corresponding author.Center for Quantitative Biology, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, China; Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, China; School of Physics, Peking University, Beijing, 100871, China; Corresponding author. Center for Quantitative Biology, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China.Most of microbe cells spend the majority of their times in quiescence due to unfavorable environmental conditions. The study of this dominant state is crucial for understanding the basic cell physiology. Retained recovery ability is a critical property of quiescent cells, which consists of two features: how long the cells can survive (the survivability) and how fast they can recover (the recovery activity). While the survivability has been extensively studied under the background of chronological aging, how the recovery activity depends on the quiescent time and what factors influence its dynamics have not been addressed quantitatively. In this work, we systematically quantified both the survivability and the recovery activity of long-lived quiescent fission yeast cells at the single cell level under various nutrient conditions. It provides the most profound evolutionary dynamics of quiescent cell regeneration ability described to date. We found that the single cell recovery time linearly increased with the starvation time before the survivability significantly declined. This linearity was robust under various nutrient conditions and the recovery speed was predetermined by the initial nutrient condition. Transcriptome profiling further revealed that quiescence states under different nutrient conditions evolve in a common trajectory but with different speed. Our results demonstrated that cellular quiescence has a continuous spectrum of depths and its physiology is greatly influenced by environmental conditions.http://www.sciencedirect.com/science/article/pii/S2405844024025891Long-term quiescenceRecovery activityDynamicsFission yeastNitrogen starvationSingle-cell study
spellingShingle Qi Liu
Nan Sheng
Zhiwen Zhang
Chenjun He
Yao Zhao
Haoyuan Sun
Jianguo Chen
Xiaojing Yang
Chao Tang
Initial nutrient condition determines the recovery speed of quiescent cells in fission yeast
Heliyon
Long-term quiescence
Recovery activity
Dynamics
Fission yeast
Nitrogen starvation
Single-cell study
title Initial nutrient condition determines the recovery speed of quiescent cells in fission yeast
title_full Initial nutrient condition determines the recovery speed of quiescent cells in fission yeast
title_fullStr Initial nutrient condition determines the recovery speed of quiescent cells in fission yeast
title_full_unstemmed Initial nutrient condition determines the recovery speed of quiescent cells in fission yeast
title_short Initial nutrient condition determines the recovery speed of quiescent cells in fission yeast
title_sort initial nutrient condition determines the recovery speed of quiescent cells in fission yeast
topic Long-term quiescence
Recovery activity
Dynamics
Fission yeast
Nitrogen starvation
Single-cell study
url http://www.sciencedirect.com/science/article/pii/S2405844024025891
work_keys_str_mv AT qiliu initialnutrientconditiondeterminestherecoveryspeedofquiescentcellsinfissionyeast
AT nansheng initialnutrientconditiondeterminestherecoveryspeedofquiescentcellsinfissionyeast
AT zhiwenzhang initialnutrientconditiondeterminestherecoveryspeedofquiescentcellsinfissionyeast
AT chenjunhe initialnutrientconditiondeterminestherecoveryspeedofquiescentcellsinfissionyeast
AT yaozhao initialnutrientconditiondeterminestherecoveryspeedofquiescentcellsinfissionyeast
AT haoyuansun initialnutrientconditiondeterminestherecoveryspeedofquiescentcellsinfissionyeast
AT jianguochen initialnutrientconditiondeterminestherecoveryspeedofquiescentcellsinfissionyeast
AT xiaojingyang initialnutrientconditiondeterminestherecoveryspeedofquiescentcellsinfissionyeast
AT chaotang initialnutrientconditiondeterminestherecoveryspeedofquiescentcellsinfissionyeast