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De novo emergence of adaptive membrane proteins from thymine-rich intergenic sequences

Nikolaos Vakirlis, Omer Acar, Brian Hsu, Nelson Castilho Coelho, S. Branden Van Oss, Aaron Wacholder, Kate Medetgul-Ernar, John Iannotta, Aoife McLysaght, Carlos J. Camacho, Allyson F. O’Donnell, Trey Ideker, View ORCID ProfileAnne-Ruxandra Carvunis
doi: https://doi.org/10.1101/621532
Nikolaos Vakirlis
1Smurfit Institute of Genetics, Trinity College Dublin, University of Dublin, Dublin 2, Ireland
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Omer Acar
2Department of Computational and Systems Biology, Pittsburgh Center for Evolutionary Biology and Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, United States
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Brian Hsu
3Department of Medicine, Division of Medical Genetics, University of California San Diego, La Jolla, CA 92093, United States
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Nelson Castilho Coelho
2Department of Computational and Systems Biology, Pittsburgh Center for Evolutionary Biology and Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, United States
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S. Branden Van Oss
2Department of Computational and Systems Biology, Pittsburgh Center for Evolutionary Biology and Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, United States
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Aaron Wacholder
2Department of Computational and Systems Biology, Pittsburgh Center for Evolutionary Biology and Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, United States
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Kate Medetgul-Ernar
3Department of Medicine, Division of Medical Genetics, University of California San Diego, La Jolla, CA 92093, United States
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John Iannotta
2Department of Computational and Systems Biology, Pittsburgh Center for Evolutionary Biology and Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, United States
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Aoife McLysaght
1Smurfit Institute of Genetics, Trinity College Dublin, University of Dublin, Dublin 2, Ireland
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Carlos J. Camacho
2Department of Computational and Systems Biology, Pittsburgh Center for Evolutionary Biology and Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, United States
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Allyson F. O’Donnell
4Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, United States
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  • For correspondence: anc201@pitt.edu tideker@ad.ucsd.edu allyod@pitt.edu
Trey Ideker
3Department of Medicine, Division of Medical Genetics, University of California San Diego, La Jolla, CA 92093, United States
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  • For correspondence: anc201@pitt.edu tideker@ad.ucsd.edu allyod@pitt.edu
Anne-Ruxandra Carvunis
2Department of Computational and Systems Biology, Pittsburgh Center for Evolutionary Biology and Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, United States
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  • ORCID record for Anne-Ruxandra Carvunis
  • For correspondence: anc201@pitt.edu tideker@ad.ucsd.edu allyod@pitt.edu
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Summary

Recent evidence demonstrates that novel protein-coding genes can arise de novo from intergenic loci. This evolutionary innovation is thought to be facilitated by the pervasive translation of intergenic transcripts, which exposes a reservoir of variable polypeptides to natural selection. Do intergenic translation events yield polypeptides with useful biochemical capacities? The answer to this question remains controversial. Here, we systematically characterized how de novo emerging coding sequences impact fitness. In budding yeast, overexpression of these sequences was enriched in beneficial effects, while their disruption was generally inconsequential. We found that beneficial emerging sequences have a strong tendency to encode putative transmembrane proteins, which appears to stem from a cryptic propensity for transmembrane signals throughout thymine-rich intergenic regions of the genome. These findings suggest that novel genes with useful biochemical capacities, such as transmembrane domains, tend to evolve de novo within intergenic loci that already harbored a blueprint for these capacities.

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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 4.0 International license.
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Posted April 29, 2019.
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De novo emergence of adaptive membrane proteins from thymine-rich intergenic sequences
Nikolaos Vakirlis, Omer Acar, Brian Hsu, Nelson Castilho Coelho, S. Branden Van Oss, Aaron Wacholder, Kate Medetgul-Ernar, John Iannotta, Aoife McLysaght, Carlos J. Camacho, Allyson F. O’Donnell, Trey Ideker, Anne-Ruxandra Carvunis
bioRxiv 621532; doi: https://doi.org/10.1101/621532
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De novo emergence of adaptive membrane proteins from thymine-rich intergenic sequences
Nikolaos Vakirlis, Omer Acar, Brian Hsu, Nelson Castilho Coelho, S. Branden Van Oss, Aaron Wacholder, Kate Medetgul-Ernar, John Iannotta, Aoife McLysaght, Carlos J. Camacho, Allyson F. O’Donnell, Trey Ideker, Anne-Ruxandra Carvunis
bioRxiv 621532; doi: https://doi.org/10.1101/621532

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