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Evolution of resilience in protein interactomes across the tree of life

Marinka Zitnik, Rok Sosič, Marcus W. Feldman, Jure Leskovec
doi: https://doi.org/10.1101/454033
Marinka Zitnik
aDepartment of Computer Science, Stanford University, Stanford, CA 94305, USA
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Rok Sosič
aDepartment of Computer Science, Stanford University, Stanford, CA 94305, USA
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Marcus W. Feldman
bDepartment of Biology, Stanford University, Stanford, CA 94305, USA
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  • For correspondence: mfeldman@stanford.edu jure@cs.stanford.com
Jure Leskovec
aDepartment of Computer Science, Stanford University, Stanford, CA 94305, USA
cChan Zuckerberg Biohub, San Francisco, CA 94158, USA
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  • For correspondence: mfeldman@stanford.edu jure@cs.stanford.com
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Abstract

Phenotype robustness to environmental fluctuations is a common biological phenomenon. Although most phenotypes involve multiple proteins that interact with each other, the basic principles of how such interactome networks respond to environmental unpredictability and change during evolution are largely unknown. Here we study interactomes of 1,840 species across the tree of life involving a total of 8,762,166 protein-protein interactions. Our study focuses on the resilience of interactomes to network failures and finds that interactomes become more resilient during evolution, indicating that a species’ position in the tree of life is predictive of how robust its interactome is to network failures. In bacteria, we find that a more resilient interactome is in turn associated with the greater ability of the organism to survive in a more complex, variable and competitive environment. We find that at the protein family level, proteins exhibit a coordinated rewiring of interactions over time and that a resilient interactome arises through gradual change of the network topology. Our findings have implications for understanding molecular network structure both in the context of evolution and environment.

Significance Statement The interactome network of protein-protein interactions captures the structure of molecular machinery that underlies organismal complexity. The resilience to network failures is a critical property of the interactome as the breakdown of interactions may lead to cell death or disease. By studying interactomes from 1,840 species across the tree of life, we find that evolution leads to more resilient interactomes, providing evidence for a longstanding hypothesis that interactomes evolve favoring robustness against network failures. We find that a highly resilient interactome has a beneficial impact on the organism’s survival in complex, variable, and competitive habitats. Our findings reveal how interactomes change through evolution and how these changes affect their response to environmental unpredictability.

Footnotes

  • M.Z. performed the statistical analysis. M.Z., R.S., M.W.F., and J.L. jointly analyzed the results and wrote the paper.

  • The authors declare no conflict of interest.

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-NC-ND 4.0 International license.
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Posted December 13, 2018.
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Evolution of resilience in protein interactomes across the tree of life
Marinka Zitnik, Rok Sosič, Marcus W. Feldman, Jure Leskovec
bioRxiv 454033; doi: https://doi.org/10.1101/454033
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Evolution of resilience in protein interactomes across the tree of life
Marinka Zitnik, Rok Sosič, Marcus W. Feldman, Jure Leskovec
bioRxiv 454033; doi: https://doi.org/10.1101/454033

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