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The Phage-shock-protein (PSP) Envelope Stress Response: Discovery of Novel Partners and Evolutionary History

View ORCID ProfileJanani Ravi, View ORCID ProfileVivek Anantharaman, Samuel Zorn Chen, Pratik Datta, View ORCID ProfileL Aravind, View ORCID ProfileMaria Laura Gennaro
doi: https://doi.org/10.1101/2020.09.24.301986
Janani Ravi
1Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, MI, USA
2Public Health Research Institute, Rutgers University, Newark, NJ, USA
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  • For correspondence: janani@msu.edu aravind@nih.gov marila.gennaro@rutgers.edu
Vivek Anantharaman
3National Center for Biotechnology Information, National Institutes of Health, Bethesda, MD, USA
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Samuel Zorn Chen
1Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, MI, USA
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Pratik Datta
2Public Health Research Institute, Rutgers University, Newark, NJ, USA
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L Aravind
3National Center for Biotechnology Information, National Institutes of Health, Bethesda, MD, USA
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  • For correspondence: janani@msu.edu aravind@nih.gov marila.gennaro@rutgers.edu
Maria Laura Gennaro
2Public Health Research Institute, Rutgers University, Newark, NJ, USA
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  • ORCID record for Maria Laura Gennaro
  • For correspondence: janani@msu.edu aravind@nih.gov marila.gennaro@rutgers.edu
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Abstract

The phage shock protein (PSP) systems orchestrate a conserved stress response function by stabilizing the cell membrane and protecting bacteria from envelope stress. The full repertoire of PSP components remains poorly characterized. We combined comparative genomics and protein sequence-structure-function analyses to systematically identify homologs, phyletic patterns, domain architectures, and gene neighborhoods to trace the evolution of PSP components across the tree of life. This approach showed that the core component PspA/Snf7 (Psp/ESCRT systems) was present in the Last Universal Common Ancestor and that different clades co-opted a diverse range of partners to constitute distinct PSP systems. We identified several novel partners of the PSP system: (i) the Toastrack domain, which likely facilitates assembling diverse sub-membrane stress-sensing and signaling complexes, (ii) the newly-defined HAAS–PadR-like transcription regulator pair system, and (iii) multiple independent associations with ATPase or CesT/Tir-like chaperones, and Band-7 domain proteins that likely mediate sub-membrane dynamics. Our work also uncovered links between the PSP components and diverse SHOCT-like domains, suggesting a role in assembling membrane-associated complexes of proteins with disparate biochemical functions. Tracing the evolution of Psp cognate proteins provides new insights into the functions of the system and helps predict previously uncharacterized, often lineage-specific, membrane-dynamics and stress-response systems. The conservation of PSP systems across bacterial phyla emphasizes the importance of this stress response system in prokaryotes, while its modular diversity in various lineages indicates the emergence of lineage-specific cell-envelope structures, lifestyles, and adaptation mechanisms. The results can be accessed at https://jravilab.shinyapps.io/psp-evolution.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Updated condensed version (mBio).

  • https://jravilab.shinyapps.io/psp-evolution

Copyright 
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 4.0 International license.
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Posted June 03, 2021.
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The Phage-shock-protein (PSP) Envelope Stress Response: Discovery of Novel Partners and Evolutionary History
Janani Ravi, Vivek Anantharaman, Samuel Zorn Chen, Pratik Datta, L Aravind, Maria Laura Gennaro
bioRxiv 2020.09.24.301986; doi: https://doi.org/10.1101/2020.09.24.301986
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The Phage-shock-protein (PSP) Envelope Stress Response: Discovery of Novel Partners and Evolutionary History
Janani Ravi, Vivek Anantharaman, Samuel Zorn Chen, Pratik Datta, L Aravind, Maria Laura Gennaro
bioRxiv 2020.09.24.301986; doi: https://doi.org/10.1101/2020.09.24.301986

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