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Unraveling Oxidative Stress Resistance: Molecular Properties Govern Proteome Vulnerability

View ORCID ProfileRoger L. Chang, Julian A. Stanley, Matthew C. Robinson, Joel W. Sher, Zhanwen Li, Yujia A. Chan, Ashton R. Omdahl, Ruddy Wattiez, Adam Godzik, Sabine Matallana-Surget
doi: https://doi.org/10.1101/2020.03.09.983213
Roger L. Chang
1Department of Systems Biology, Blavatnik Institute at Harvard Medical School, Boston, MA 02115, USA
2Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA 02115, USA
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  • ORCID record for Roger L. Chang
  • For correspondence: sabine.matallanasurget@stir.ac.uk roger_chang@hms.harvard.edu
Julian A. Stanley
1Department of Systems Biology, Blavatnik Institute at Harvard Medical School, Boston, MA 02115, USA
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Matthew C. Robinson
1Department of Systems Biology, Blavatnik Institute at Harvard Medical School, Boston, MA 02115, USA
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Joel W. Sher
1Department of Systems Biology, Blavatnik Institute at Harvard Medical School, Boston, MA 02115, USA
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Zhanwen Li
3Division of Biomedical Sciences, University of California Riverside School of Medicine, Riverside, CA 92521, USA
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Yujia A. Chan
1Department of Systems Biology, Blavatnik Institute at Harvard Medical School, Boston, MA 02115, USA
2Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA 02115, USA
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Ashton R. Omdahl
1Department of Systems Biology, Blavatnik Institute at Harvard Medical School, Boston, MA 02115, USA
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Ruddy Wattiez
4Department of Proteomics and Microbiology, Research Institute for Biosciences, University of Mons, Mons B-7000, Belgium
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Adam Godzik
3Division of Biomedical Sciences, University of California Riverside School of Medicine, Riverside, CA 92521, USA
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Sabine Matallana-Surget
5Division of Biological and Environmental Sciences, Faculty of Natural Sciences, University of Stirling, Stirling FK9 4LA, Scotland UK
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  • For correspondence: sabine.matallanasurget@stir.ac.uk roger_chang@hms.harvard.edu
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Abstract:

Oxidative stress alters cell viability, from microorganism irradiation sensitivity to human aging and neurodegeneration. Deleterious effects of protein carbonylation by reactive oxygen species (ROS) make understanding molecular properties determining ROS-susceptibility essential. The radiation-resistant bacterium Deinococcus radiodurans accumulates less carbonylation than sensitive organisms, making it a key model for deciphering properties governing oxidative stress resistance. We integrated shotgun redox proteomics, structural systems biology, and machine learning to resolve properties determining protein damage by γ-irradiation in Escherichia coli and D. radiodurans at multiple scales. Local accessibility, charge, and lysine enrichment accurately predict ROS-susceptibility. Lysine, methionine, and cysteine usage also contribute to ROS-resistance of the D. radiodurans proteome. Our model predicts proteome maintenance machinery and proteins protecting against ROS are more resistant in D. radiodurans. Our findings substantiate that protein-intrinsic protection impacts oxidative stress resistance, identifying causal molecular properties.

One Sentence Summary Proteins differ in intrinsic susceptibility to oxidation, a mode of evolutionary adaptation for stress tolerance in bacteria.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 09, 2020.
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Unraveling Oxidative Stress Resistance: Molecular Properties Govern Proteome Vulnerability
Roger L. Chang, Julian A. Stanley, Matthew C. Robinson, Joel W. Sher, Zhanwen Li, Yujia A. Chan, Ashton R. Omdahl, Ruddy Wattiez, Adam Godzik, Sabine Matallana-Surget
bioRxiv 2020.03.09.983213; doi: https://doi.org/10.1101/2020.03.09.983213
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Unraveling Oxidative Stress Resistance: Molecular Properties Govern Proteome Vulnerability
Roger L. Chang, Julian A. Stanley, Matthew C. Robinson, Joel W. Sher, Zhanwen Li, Yujia A. Chan, Ashton R. Omdahl, Ruddy Wattiez, Adam Godzik, Sabine Matallana-Surget
bioRxiv 2020.03.09.983213; doi: https://doi.org/10.1101/2020.03.09.983213

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