Divergent Molecular Responses to Heavy Water in <i>Arabidopsis thaliana</i> Compared to Bacteria and Yeast

Heavy water (D<sub>2</sub>O) is scarce in nature, and despite its physical similarity to water, D<sub>2</sub>O disrupts cellular function due to the isotope effect. While microbes can survive in nearly pure D<sub>2</sub>O, eukaryotes such as <i>Arabidopsis t...

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Main Authors: Pengxi Wang, Jan Novák, Romana Kopecká, Petr Čičmanec, Martin Černý
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/13/22/3121
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author Pengxi Wang
Jan Novák
Romana Kopecká
Petr Čičmanec
Martin Černý
author_facet Pengxi Wang
Jan Novák
Romana Kopecká
Petr Čičmanec
Martin Černý
author_sort Pengxi Wang
collection DOAJ
description Heavy water (D<sub>2</sub>O) is scarce in nature, and despite its physical similarity to water, D<sub>2</sub>O disrupts cellular function due to the isotope effect. While microbes can survive in nearly pure D<sub>2</sub>O, eukaryotes such as <i>Arabidopsis thaliana</i> are more sensitive and are unable to survive higher concentrations of D<sub>2</sub>O. To explore the underlying molecular mechanisms for these differences, we conducted a comparative proteomic analysis of <i>E. coli</i>, <i>S. cerevisiae</i>, and <i>Arabidopsis</i> after 180 min of growth in a D<sub>2</sub>O-supplemented media. Shared adaptive mechanisms across these species were identified, including changes in ribosomal protein abundances, accumulation of chaperones, and altered metabolism of polyamines and amino acids. However, <i>Arabidopsis</i> exhibited unique vulnerabilities, such as a muted stress response, lack of rapid activation of reactive oxygen species metabolism, and depletion of stress phytohormone abscisic acid signaling components. Experiments with mutants show that modulating the HSP70 pool composition may promote D<sub>2</sub>O resilience. Additionally, <i>Arabidopsis</i> rapidly incorporated deuterium into sucrose, indicating that photosynthesis facilitates deuterium intake. These findings provide valuable insights into the molecular mechanisms that dictate differential tolerance to D<sub>2</sub>O across species and lay the groundwork for further studies on the biological effects of uncommon isotopes, with potential implications for biotechnology and environmental science.
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spelling doaj-art-4274aeb097ab4265b33580362a73e83a2025-08-20T02:05:01ZengMDPI AGPlants2223-77472024-11-011322312110.3390/plants13223121Divergent Molecular Responses to Heavy Water in <i>Arabidopsis thaliana</i> Compared to Bacteria and YeastPengxi Wang0Jan Novák1Romana Kopecká2Petr Čičmanec3Martin Černý4Department of Molecular Biology and Radiobiology, Faculty of AgriSciences, Mendel University in Brno, 61300 Brno, Czech RepublicDepartment of Molecular Biology and Radiobiology, Faculty of AgriSciences, Mendel University in Brno, 61300 Brno, Czech RepublicDepartment of Molecular Biology and Radiobiology, Faculty of AgriSciences, Mendel University in Brno, 61300 Brno, Czech RepublicDepartment of Molecular Biology and Radiobiology, Faculty of AgriSciences, Mendel University in Brno, 61300 Brno, Czech RepublicDepartment of Molecular Biology and Radiobiology, Faculty of AgriSciences, Mendel University in Brno, 61300 Brno, Czech RepublicHeavy water (D<sub>2</sub>O) is scarce in nature, and despite its physical similarity to water, D<sub>2</sub>O disrupts cellular function due to the isotope effect. While microbes can survive in nearly pure D<sub>2</sub>O, eukaryotes such as <i>Arabidopsis thaliana</i> are more sensitive and are unable to survive higher concentrations of D<sub>2</sub>O. To explore the underlying molecular mechanisms for these differences, we conducted a comparative proteomic analysis of <i>E. coli</i>, <i>S. cerevisiae</i>, and <i>Arabidopsis</i> after 180 min of growth in a D<sub>2</sub>O-supplemented media. Shared adaptive mechanisms across these species were identified, including changes in ribosomal protein abundances, accumulation of chaperones, and altered metabolism of polyamines and amino acids. However, <i>Arabidopsis</i> exhibited unique vulnerabilities, such as a muted stress response, lack of rapid activation of reactive oxygen species metabolism, and depletion of stress phytohormone abscisic acid signaling components. Experiments with mutants show that modulating the HSP70 pool composition may promote D<sub>2</sub>O resilience. Additionally, <i>Arabidopsis</i> rapidly incorporated deuterium into sucrose, indicating that photosynthesis facilitates deuterium intake. These findings provide valuable insights into the molecular mechanisms that dictate differential tolerance to D<sub>2</sub>O across species and lay the groundwork for further studies on the biological effects of uncommon isotopes, with potential implications for biotechnology and environmental science.https://www.mdpi.com/2223-7747/13/22/3121stress responseproteomeROS metabolismdeuterium oxideadaptationHSP70
spellingShingle Pengxi Wang
Jan Novák
Romana Kopecká
Petr Čičmanec
Martin Černý
Divergent Molecular Responses to Heavy Water in <i>Arabidopsis thaliana</i> Compared to Bacteria and Yeast
Plants
stress response
proteome
ROS metabolism
deuterium oxide
adaptation
HSP70
title Divergent Molecular Responses to Heavy Water in <i>Arabidopsis thaliana</i> Compared to Bacteria and Yeast
title_full Divergent Molecular Responses to Heavy Water in <i>Arabidopsis thaliana</i> Compared to Bacteria and Yeast
title_fullStr Divergent Molecular Responses to Heavy Water in <i>Arabidopsis thaliana</i> Compared to Bacteria and Yeast
title_full_unstemmed Divergent Molecular Responses to Heavy Water in <i>Arabidopsis thaliana</i> Compared to Bacteria and Yeast
title_short Divergent Molecular Responses to Heavy Water in <i>Arabidopsis thaliana</i> Compared to Bacteria and Yeast
title_sort divergent molecular responses to heavy water in i arabidopsis thaliana i compared to bacteria and yeast
topic stress response
proteome
ROS metabolism
deuterium oxide
adaptation
HSP70
url https://www.mdpi.com/2223-7747/13/22/3121
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AT jannovak divergentmolecularresponsestoheavywateriniarabidopsisthalianaicomparedtobacteriaandyeast
AT romanakopecka divergentmolecularresponsestoheavywateriniarabidopsisthalianaicomparedtobacteriaandyeast
AT petrcicmanec divergentmolecularresponsestoheavywateriniarabidopsisthalianaicomparedtobacteriaandyeast
AT martincerny divergentmolecularresponsestoheavywateriniarabidopsisthalianaicomparedtobacteriaandyeast