Evolutionary interplay between structure, energy and epistasis in the coat protein of the ϕX174 phage family

Journal of the Royal Society, Interface
Rodrigo A F RedondoJonathan P Bollback

Abstract

Viral capsids are structurally constrained by interactions among the amino acids (AAs) of their constituent proteins. Therefore, epistasis is expected to evolve among physically interacting sites and to influence the rates of substitution. To study the evolution of epistasis, we focused on the major structural protein of the ϕX174 phage family by first reconstructing the ancestral protein sequences of 18 species using a Bayesian statistical framework. The inferred ancestral reconstruction differed at eight AAs, for a total of 256 possible ancestral haplotypes. For each ancestral haplotype and the extant species, we estimated, in silico, the distribution of free energies and epistasis of the capsid structure. We found that free energy has not significantly increased but epistasis has. We decomposed epistasis up to fifth order and found that higher-order epistasis sometimes compensates pairwise interactions making the free energy seem additive. The dN/dS ratio is low, suggesting strong purifying selection, and that structure is under stabilizing selection. We synthesized phages carrying ancestral haplotypes of the coat protein gene and measured their fitness experimentally. Our findings indicate that stabilizing mutations can hav...Continue Reading

References

Nov 16, 1978·Nature·G N GodsonJ C Fiddes
Feb 24, 1977·Nature·F SangerM Smith
Sep 18, 1990·Biochemistry·J A Wells
Dec 18, 1986·Nature·T ImanakaM Takagi
Jul 1, 1974·Proceedings of the National Academy of Sciences of the United States of America·M Kimura, T Ohta
Jun 1, 2000·Molecular Biology and Evolution·J J BullH A Wichman
Dec 29, 2000·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·H A WichmanJ J Bull
Dec 12, 2001·Journal of Virology·Edward C Holmes, Andrés Moya
Jun 25, 2002·Journal of Molecular Biology·Raphael GueroisLuis Serrano
Jul 15, 2003·The American Naturalist·Joachim HermissonGünter P Wagner
Oct 15, 2003·Journal of Molecular Biology·Ariel A Di NardoAlan R Davidson
Jul 12, 2005·Proceedings of the National Academy of Sciences of the United States of America·Joost SchymkowitzLuis Serrano
Jan 24, 2006·Journal of Bacteriology·D R RokytaH A Wichman
May 8, 2007·Journal of Molecular Biology·Nobuhiko TokurikiDan S Tawfik
May 8, 2007·Molecular Biology and Evolution·Ziheng Yang
Jul 20, 2007·Nature Reviews. Genetics·Adam Eyre-Walker, Peter D Keightley
Aug 19, 2007·Science·Eric A OrtlundJoseph W Thornton
Aug 28, 2007·Genetics·Michael M DesaiMarcus W Feldman
May 9, 2008·PLoS Computational Biology·Nobuhiko TokurikiDan S Tawfik
Apr 22, 2009·PLoS Computational Biology·Jesse D Bloom, Matthew J Glassman
May 29, 2009·Proceedings of the National Academy of Sciences of the United States of America·Lucia A HindorffTeri A Manolio
Jun 24, 2009·Nature Reviews. Genetics·H Allen Orr
Mar 24, 2010·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·James F Crow
Apr 22, 2010·Proteins·Kresten Lindorff-LarsenDavid E Shaw
May 14, 2010·PLoS Computational Biology·Raul MendezUgo Bastolla
Dec 29, 2010·Methods in Enzymology·Andrew Leaver-FayPhilip Bradley
Nov 19, 2011·Proteins·Sean Burke, Ron Elber
Jan 17, 2012·American Journal of Human Genetics·Peter M VisscherJian Yang
Feb 24, 2012·Systematic Biology·Fredrik RonquistJohn P Huelsenbeck
May 2, 2012·Proceedings of the National Academy of Sciences of the United States of America·David D PollockRichard A Goldstein
Jul 5, 2012·PLoS Computational Biology·Claus O Wilke
Oct 9, 2012·Nature·Richard N McLaughlinRama Ranganathan
Oct 16, 2012·Nature·Michael S BreenFyodor A Kondrashov
Oct 31, 2012·Evolution; International Journal of Organic Evolution·Pedro F ValeSylvain Gandon
Feb 6, 2013·Proceedings of the National Academy of Sciences of the United States of America·Chungoo ParkJianzhi Zhang
Jun 27, 2013·Proceedings of the National Academy of Sciences of the United States of America·Michael J HarmsJoseph W Thornton
Jul 19, 2013·Nature Reviews. Genetics·Michael J Harms, Joseph W Thornton
Dec 3, 2013·Current Opinion in Genetics & Development·Daniel M WeinreichRobert B Heckendorn
Dec 11, 2013·Proceedings of the National Academy of Sciences of the United States of America·Orr AshenbergJesse D Bloom
Apr 8, 2014·Proceedings of the National Academy of Sciences of the United States of America·David D Pollock, Richard A Goldstein
May 21, 2014·Proceedings of the National Academy of Sciences of the United States of America·Jakub Otwinowski, Joshua B Plotkin
Aug 29, 2014·Journal of the Royal Society, Interface·Tobias Sikosek, Hue Sun Chan
Jan 20, 2016·Nature Reviews. Genetics·Julian EchaveClaus O Wilke

Citations

Jan 9, 2020·Journal of the Royal Society, Interface·Axel PetzoldSonia O'Connor

Related Concepts

Bacteriophage phi X 174
Selection, Genetic
Evolution, Molecular
Capsid Proteins
Bacteriophages
Epistasis, Genetic
Genes
Viral Structural Proteins
Site
Reconstructive Surgical Procedures

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