The thermostability and specificity of ancient proteins.

Were ancient proteins systematically different than modern proteins? The answer to this question is profoundly important, shaping how we understand the origins of protein biochemical, biophysical, and functional properties. Ancestral sequence reconstruction (ASR), a phylogenetic approach to infer the sequences of ancestral proteins, may reveal such trends. We discuss two proposed trends: a transition from higher to lower thermostability and a tendency for proteins to acquire higher specificity over time. We review the evidence for elevated ancestral thermostability and discuss its possible origins in a changing environmental temperature and/or reconstruction bias. We also conclude that there is, as yet, insufficient data to support a trend from promiscuity to specificity. Finally, we propose future work to understand these proposed evolutionary trends.

[1]  Eugene I Shakhnovich,et al.  Sequence correlations shape protein promiscuity. , 2011, The Journal of chemical physics.

[2]  R. Goldstein,et al.  Amino acid coevolution induces an evolutionary Stokes shift , 2012, Proceedings of the National Academy of Sciences.

[3]  Marc A Suchard,et al.  Stability-mediated epistasis constrains the evolution of an influenza protein , 2013, eLife.

[4]  S. Govindarajan,et al.  Palaeotemperature trend for Precambrian life inferred from resurrected proteins , 2008, Nature.

[5]  M. Laub,et al.  Evolving New Protein-Protein Interaction Specificity through Promiscuous Intermediates , 2015, Cell.

[6]  D. M. Taverna,et al.  Why are proteins marginally stable? , 2002, Proteins.

[7]  D. Theobald,et al.  An atomic-resolution view of neofunctionalization in the evolution of apicomplexan lactate dehydrogenases , 2014, eLife.

[8]  Adrian W. R. Serohijos,et al.  Positively Selected Sites in Cetacean Myoglobins Contribute to Protein Stability , 2013, PLoS Comput. Biol..

[9]  Richard A. Goldstein,et al.  Nonadaptive Amino Acid Convergence Rates Decrease over Time , 2015, Molecular biology and evolution.

[10]  Kathryn M Hart,et al.  Thermodynamic System Drift in Protein Evolution , 2014, PLoS Biology.

[11]  P. Kosuri,et al.  Single-molecule paleoenzymology probes the chemistry of resurrected enzymes , 2011, Nature Structural &Molecular Biology.

[12]  J. A. Gavira,et al.  Phenotypic comparisons of consensus variants versus laboratory resurrections of Precambrian proteins , 2014, Proteins.

[13]  C. Henneberger,et al.  Construction of a robust and sensitive arginine biosensor through ancestral protein reconstruction , 2015, Protein science : a publication of the Protein Society.

[14]  Victor Hanson-Smith,et al.  Ancestral resurrection reveals evolutionary mechanisms of kinase plasticity , 2014, eLife.

[15]  Adi Stern,et al.  Assessing the prediction fidelity of ancestral reconstruction by a library approach. , 2015, Protein engineering, design & selection : PEDS.

[16]  Juhan Kim,et al.  Inhibitory cross-talk upon introduction of a new metabolic pathway into an existing metabolic network , 2012, Proceedings of the National Academy of Sciences.

[17]  Z. Weng,et al.  Ancestral and consensus envelope immunogens for HIV-1 subtype C. , 2006, Virology.

[18]  I. Sumara,et al.  Using ancient protein kinases to unravel a modern cancer drug’s mechanism , 2015, Science.

[19]  Orit Peleg,et al.  Evolution of specificity in protein-protein interactions. , 2014, Biophysical journal.

[20]  R. Jensen.  Enzyme recruitment in evolution of new function. , 1976, Annual review of microbiology.

[21]  Brian W. Matthews,et al.  Ancestral lysozymes reconstructed, neutrality tested, and thermostability linked to hydrocarbon packing , 1990, Nature.

[22]  Paul D. Williams,et al.  Assessing the Accuracy of Ancestral Protein Reconstruction Methods , 2006, PLoS Comput. Biol..

[23]  Jiunn R Chen,et al.  PDZ Domain Binding Selectivity Is Optimized Across the Mouse Proteome , 2007, Science.

[24]  Eric A. Ortlund,et al.  Evolution of Minimal Specificity and Promiscuity in Steroid Hormone Receptors , 2012, PLoS genetics.

[25]  D. Gresham,et al.  Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments , 2014, PLoS genetics.

[26]  S. Tans,et al.  Breaking evolutionary constraint with a tradeoff ratchet , 2015, Proceedings of the National Academy of Sciences.

[27]  S. Akanuma,et al.  Experimental evidence for the thermophilicity of ancestral life , 2013, Proceedings of the National Academy of Sciences.

[28]  M. Gouy,et al.  Toward More Accurate Ancestral Protein Genotype–Phenotype Reconstructions with the Use of Species Tree-Aware Gene Trees , 2014, Molecular biology and evolution.

[29]  M. Harms,et al.  Analyzing protein structure and function using ancestral gene reconstruction. , 2010, Current opinion in structural biology.

[30]  Megan F. Cole,et al.  Utilizing natural diversity to evolve protein function: applications towards thermostability. , 2011, Current opinion in chemical biology.

[31]  Andrew J. Bannister,et al.  Acetylation of histone H3 at lysine 64 regulates nucleosome dynamics and facilitates transcription , 2014, eLife.

[32]  J. M. Sanchez-Ruiz,et al.  Thermostable and promiscuous Precambrian proteins. , 2014, Environmental microbiology.

[33]  E. Ortlund,et al.  Evolution of DNA Specificity in a Transcription Factor Family Produced a New Gene Regulatory Module , 2014, Cell.

[34]  Ke Liu,et al.  A despecialization step underlying evolution of a family of serine proteases. , 2003, Molecular cell.

[35]  C. Ó’Fágáin,et al.  Stability properties of an ancient plant peroxidase. , 2014, Biochimie.

[36]  Alexander J. Stewart,et al.  The evolution of complex gene regulation by low-specificity binding sites , 2012, Proceedings of the Royal Society B: Biological Sciences.

[37]  Feng Gao,et al.  Diversity Considerations in HIV-1 Vaccine Selection , 2002, Science.

[38]  K. Verstrepen,et al.  Reconstruction of Ancestral Metabolic Enzymes Reveals Molecular Mechanisms Underlying Evolutionary Innovation through Gene Duplication , 2012, PLoS biology.

[39]  S. Akanuma,et al.  Phylogeny-based design of a B-subunit of DNA gyrase and its ATPase domain using a small set of homologous amino acid sequences. , 2011, Journal of molecular biology.

[40]  Satoshi Akanuma,et al.  Robustness of predictions of extremely thermally stable proteins in ancient organisms , 2015, Evolution; international journal of organic evolution.

[41]  Colin J Jackson,et al.  Ancestral Protein Reconstruction Yields Insights into Adaptive Evolution of Binding Specificity in Solute-Binding Proteins. , 2016, Cell chemical biology.

[42]  V. Arcus,et al.  On the origin and evolution of thermophily: reconstruction of functional precambrian enzymes from ancestors of Bacillus. , 2012, Molecular biology and evolution.

[43]  Kenneth H. Wolfe,et al.  Turning a hobby into a job: How duplicated genes find new functions , 2008, Nature Reviews Genetics.

[44]  Linus Pauling,et al.  Chemical Paleogenetics. Molecular "Restoration Studies" of Extinct Forms of Life. , 1963 .

[45]  I. Kobayashi,et al.  Evolution of sequence recognition by restriction-modification enzymes: selective pressure for specificity decrease. , 2000, Molecular biology and evolution.

[46]  M. Gromiha,et al.  Important amino acid properties for enhanced thermostability from mesophilic to thermophilic proteins. , 1999, Biophysical chemistry.

[47]  S. Hedges,et al.  A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land , 2004, BMC Evolutionary Biology.

[48]  Bryan D. Kolaczkowski,et al.  Robustness of Ancestral Sequence Reconstruction to Phylogenetic Uncertainty , 2010, Molecular biology and evolution.

[49]  Gary D. Bader,et al.  Coevolution of PDZ domain-ligand interactions analyzed by high-throughput phage display and deep sequencing. , 2010, Molecular bioSystems.

[50]  Dan S. Tawfik,et al.  Intense neutral drifts yield robust and evolvable consensus proteins. , 2008, Journal of molecular biology.

[51]  J. A. Gavira,et al.  Hyperstability and substrate promiscuity in laboratory resurrections of Precambrian β-lactamases. , 2013, Journal of the American Chemical Society.

[52]  S. Ravanel,et al.  Molecular Evolution of the Substrate Specificity of Chloroplastic Aldolases/Rubisco Lysine Methyltransferases in Plants. , 2016, Molecular plant.

[53]  E. Ortlund,et al.  An epistatic ratchet constrains the direction of glucocorticoid receptor evolution , 2009, Nature.

[54]  A. Force,et al.  The probability of duplicate gene preservation by subfunctionalization. , 2000, Genetics.