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

Nikolaos Vakirlis, Omer Acar, Brian Hsu, Nelson Castilho Coelho, S. Branden Van Oss, Aaron Wacholder, Kate Medetgul-Ernar, Ray W. Bowman, Cameron P. Hines, John Iannotta, Saurin Bipin Parikh, Aoife McLysaght, Carlos J. Camacho, Allyson F. O’Donnell (), Trey Ideker () and Anne-Ruxandra Carvunis ()
Additional contact information
Nikolaos Vakirlis: University of Dublin
Omer Acar: University of Pittsburgh
Brian Hsu: University of California San Diego
Nelson Castilho Coelho: University of Pittsburgh
S. Branden Van Oss: University of Pittsburgh
Aaron Wacholder: University of Pittsburgh
Kate Medetgul-Ernar: University of California San Diego
Ray W. Bowman: University of Pittsburgh
Cameron P. Hines: University of California San Diego
John Iannotta: University of Pittsburgh
Saurin Bipin Parikh: University of Pittsburgh
Aoife McLysaght: University of Dublin
Carlos J. Camacho: University of Pittsburgh
Allyson F. O’Donnell: University of Pittsburgh
Trey Ideker: University of California San Diego
Anne-Ruxandra Carvunis: University of Pittsburgh

Nature Communications, 2020, vol. 11, issue 1, 1-18

Abstract: Abstract Recent evidence demonstrates that novel protein-coding genes can arise de novo from non-genic loci. This evolutionary innovation is thought to be facilitated by the pervasive translation of non-genic transcripts, which exposes a reservoir of variable polypeptides to natural selection. Here, we systematically characterize how these de novo emerging coding sequences impact fitness in budding yeast. Disruption of emerging sequences is generally inconsequential for fitness in the laboratory and in natural populations. Overexpression of emerging sequences, however, is enriched in adaptive fitness effects compared to overexpression of established genes. We find that adaptive emerging sequences tend to encode putative transmembrane domains, and that thymine-rich intergenic regions harbor a widespread potential to produce transmembrane domains. These findings, together with in-depth examination of the de novo emerging YBR196C-A locus, suggest a novel evolutionary model whereby adaptive transmembrane polypeptides emerge de novo from thymine-rich non-genic regions and subsequently accumulate changes molded by natural selection.

Date: 2020
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DOI: 10.1038/s41467-020-14500-z

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