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Title: Comparing residue clusters from thermophilic and mesophilic enzymes reveals adaptive mechanisms

Abstract

Understanding how proteins adapt to function at high temperatures is important for deciphering the energetics that dictate protein stability and folding. While multiple principles important for thermostability have been identified, we lack a unified understanding of how internal protein structural and chemical environment determine qualitative or quantitative impact of evolutionary mutations. In this work we compare equivalent clusters of spatially neighboring residues between paired thermophilic and mesophilic homologues to evaluate adaptations under the selective pressure of high temperature. We find the residue clusters in thermophilic enzymes generally display improved atomic packing compared to mesophilic enzymes, in agreement with previous research. Unlike residue clusters from mesophilic enzymes, however, thermophilic residue clusters do not have significant cavities. In addition, anchor residues found in many clusters are highly conserved with respect to atomic packing between both thermophilic and mesophilic enzymes. As a result, the improvements in atomic packing observed in thermophilic homologues are not derived from these anchor residues but from neighboring positions, which may serve to expand optimized protein core regions.

Authors:
 [1];  [2];  [1];  [2];  [1];  [1]
+ Show Author Affiliations
  1. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  2. Univ. of Colorado, Boulder, CO (United States)
Publication Date:
Research Org.:
National Renewable Energy Laboratory (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Bioenergy Technologies Office (BETO)
OSTI Identifier:
1236763
Report Number(s):
NREL/JA-2700-65616
Journal ID: ISSN 1932-6203
Grant/Contract Number:  
AC36-08GO28308
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 11; Journal Issue: 1; Related Information: PLoS One; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; thermophilic; mesophilic; enzymes; atomic packing; clusters; sequence motif analysis; enzyme structure; sequence alignment; protein structure comparison; bacillus; dehydrogenases; protein structure databases; protein domains

Citation Formats

Sammond, Deanne W., Kastelowitz, Noah, Himmel, Michael E., Yin, Hang, Crowley, Michael F., and Bomble, Yannick J. Comparing residue clusters from thermophilic and mesophilic enzymes reveals adaptive mechanisms. United States: N. p., 2016. Web. doi:10.1371/journal.pone.0145848.
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Sammond, Deanne W., Kastelowitz, Noah, Himmel, Michael E., Yin, Hang, Crowley, Michael F., & Bomble, Yannick J. Comparing residue clusters from thermophilic and mesophilic enzymes reveals adaptive mechanisms. United States. https://doi.org/10.1371/journal.pone.0145848
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Sammond, Deanne W., Kastelowitz, Noah, Himmel, Michael E., Yin, Hang, Crowley, Michael F., and Bomble, Yannick J. Thu . "Comparing residue clusters from thermophilic and mesophilic enzymes reveals adaptive mechanisms". United States. https://doi.org/10.1371/journal.pone.0145848. https://www.osti.gov/servlets/purl/1236763.
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@article{osti_1236763,
title = {Comparing residue clusters from thermophilic and mesophilic enzymes reveals adaptive mechanisms},
author = {Sammond, Deanne W. and Kastelowitz, Noah and Himmel, Michael E. and Yin, Hang and Crowley, Michael F. and Bomble, Yannick J.},
abstractNote = {Understanding how proteins adapt to function at high temperatures is important for deciphering the energetics that dictate protein stability and folding. While multiple principles important for thermostability have been identified, we lack a unified understanding of how internal protein structural and chemical environment determine qualitative or quantitative impact of evolutionary mutations. In this work we compare equivalent clusters of spatially neighboring residues between paired thermophilic and mesophilic homologues to evaluate adaptations under the selective pressure of high temperature. We find the residue clusters in thermophilic enzymes generally display improved atomic packing compared to mesophilic enzymes, in agreement with previous research. Unlike residue clusters from mesophilic enzymes, however, thermophilic residue clusters do not have significant cavities. In addition, anchor residues found in many clusters are highly conserved with respect to atomic packing between both thermophilic and mesophilic enzymes. As a result, the improvements in atomic packing observed in thermophilic homologues are not derived from these anchor residues but from neighboring positions, which may serve to expand optimized protein core regions.},
doi = {10.1371/journal.pone.0145848},
journal = {PLoS ONE},
number = 1,
volume = 11,
place = {United States},
year = {Thu Jan 07 00:00:00 EST 2016},
month = {Thu Jan 07 00:00:00 EST 2016}
}
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https://doi.org/10.1371/journal.pone.0145848
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Works referenced in this record:

Additivity of mutational effects in proteins
journal, September 1990

On the relationship between the sequence conservation and the packing density profiles of the protein complexes: Sequence Conservation and Packing Density of Protein Complexes
journal, April 2013

  • Chang, Chih-Min; Huang, Yu-Wen; Shih, Chien-Hua
  • Proteins: Structure, Function, and Bioinformatics, Vol. 81, Issue 7
  • DOI: 10.1002/prot.24268

Electrostatic contributions to the stability of hyperthermophilic proteins 1 1Edited by J. M. Thornton
journal, June 1999

Automated selection of stabilizing mutations in designed and natural proteins
journal, January 2012

  • Borgo, B.; Havranek, J. J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 5
  • DOI: 10.1073/pnas.1115172109

Protein sequence entropy is closely related to packing density and hydrophobicity
journal, February 2005

  • Liao, H.; Yeh, W.; Chiang, D.
  • Protein Engineering, Design and Selection, Vol. 18, Issue 2
  • DOI: 10.1093/protein/gzi009

Pervasive degeneracy and epistasis in a protein-protein interface
journal, February 2015

The upper limits of enzyme thermal stability
journal, July 1996

Conservation of rapid two-state folding in mesophilic, thermophilic and hyperthermophilic cold shock proteins
journal, March 1998

  • Perl, Dieter; Welker, Christine; Schindler, Thomas
  • Nature Structural Biology, Vol. 5, Issue 3
  • DOI: 10.1038/nsb0398-229

A Novel Evaluation of Residue and Protein Volumes by Means of Laguerre Tessellation
journal, April 2010

  • Esque, Jeremy; Oguey, Christophe; de Brevern, Alexandre G.
  • Journal of Chemical Information and Modeling, Vol. 50, Issue 5
  • DOI: 10.1021/ci9004892

Methionine Aminopeptidases from Mycobacterium tuberculosis as Novel Antimycobacterial Targets
journal, January 2010

Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
journal, February 2007

  • Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
  • Science, Vol. 315, Issue 5813, p. 804-807
  • DOI: 10.1126/science.1137016

Kinetics and Thermodynamics of Ligand Binding to a Molten Globular Enzyme and Its Native Counterpart
journal, October 2008

  • Vamvaca, Katherina; Jelesarov, Ilian; Hilvert, Donald
  • Journal of Molecular Biology, Vol. 382, Issue 4
  • DOI: 10.1016/j.jmb.2008.07.049

Contribution of Electrostatic Interactions, Compactness and Quaternary Structure to Protein Thermostability: Lessons from Structural Genomics of Thermotoga maritima
journal, February 2006

  • Robinson-Rechavi, Marc; Alibés, Andreu; Godzik, Adam
  • Journal of Molecular Biology, Vol. 356, Issue 2
  • DOI: 10.1016/j.jmb.2005.11.065

Hydrophobic environment is a key factor for the stability of thermophilic proteins
journal, January 2013

  • Gromiha, M. Michael; Pathak, Manish C.; Saraboji, Kadhirvel
  • Proteins: Structure, Function, and Bioinformatics, Vol. 81, Issue 4
  • DOI: 10.1002/prot.24232

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009

  • Cantarel, B. L.; Coutinho, P. M.; Rancurel, C.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn663

Increasing the thermostability of staphylococcal nuclease: implications for the origin of protein thermostability
journal, October 2000

  • Chen, Junmei; Lu, Zhiqiang; Sakon, Joshua
  • Journal of Molecular Biology, Vol. 303, Issue 2
  • DOI: 10.1006/jmbi.2000.4140

Expression, crystal structure and cellulase activity of the thermostable cellobiohydrolase Cel7A from the fungus Humicola grisea var. thermoidea
journal, August 2014

  • Momeni, Majid Haddad; Goedegebuur, Frits; Hansson, Henrik
  • Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 9
  • DOI: 10.1107/S1399004714013844

Crystal structure of endo-1,4-β-glucanase from Eisenia fetida
journal, October 2013

  • Arimori, Takao; Ito, Akihiro; Nakazawa, Masami
  • Journal of Synchrotron Radiation, Vol. 20, Issue 6
  • DOI: 10.1107/S0909049513021110

Structure-Based Design of Supercharged, Highly Thermoresistant Antibodies
journal, April 2012

Amino acid preferences for specific locations at the ends of alpha helices
journal, June 1988

Engineering chimeric thermostable GH7 cellobiohydrolases in Saccharomyces cerevisiae
journal, August 2013

  • Voutilainen, Sanni P.; Nurmi-Rantala, Susanna; Penttilä, Merja
  • Applied Microbiology and Biotechnology, Vol. 98, Issue 7
  • DOI: 10.1007/s00253-013-5177-2

Effective factors in thermostability of thermophilic proteins
journal, February 2006

Hydrophobic Effect on the Stability and Folding of a Hyperthermophilic Protein
journal, April 2008

  • Dong, Hongju; Mukaiyama, Atsushi; Tadokoro, Takashi
  • Journal of Molecular Biology, Vol. 378, Issue 1
  • DOI: 10.1016/j.jmb.2008.02.039

Exhaustive matching of the entire protein sequence database
journal, June 1992

Denatured States of Proteins
journal, June 1991

Context Dependence and Coevolution Among Amino Acid Residues in Proteins
book, January 2005

Protein structure and evolutionary history determine sequence space topology
journal, February 2005

Mechanisms for stabilisation and the maintenance of solubility in proteins from thermophiles
journal, January 2007

Native protein sequences are close to optimal for their structures
journal, September 2000

  • Kuhlman, B.; Baker, D.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 19
  • DOI: 10.1073/pnas.97.19.10383

High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis
journal, June 1989

Comparative void-volume analysis of psychrophilic and mesophilic enzymes: Structural bioinformatics of psychrophilic enzymes reveals sources of core flexibility
journal, January 2011

  • Paredes, Diana I.; Watters, Kyle; Pitman, Derek J.
  • BMC Structural Biology, Vol. 11, Issue 1
  • DOI: 10.1186/1472-6807-11-42

Coevolutionary Patterns in Cytochrome c Oxidase Subunit I Depend on Structural and Functional Context
journal, October 2007

Proteins from thermophilic and mesophilic organisms essentially do not differ in packing
journal, October 1998

Molecular insights into substrate specificity and thermal stability of a bacterial GH5-CBM27 endo-1,4-β-d-mannanase
journal, February 2012

  • Santos, Camila Ramos dos; Paiva, Joice Helena; Meza, Andreia Navarro
  • Journal of Structural Biology, Vol. 177, Issue 2
  • DOI: 10.1016/j.jsb.2011.11.021

The interpretation of protein structures: Estimation of static accessibility
journal, February 1971

Cell proliferation at 122 C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation
journal, July 2008

  • Takai, K.; Nakamura, K.; Toki, T.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 31
  • DOI: 10.1073/pnas.0712334105

Protein thermostabilization by proline substitutions
journal, June 1998

Practically Useful: What the R osetta Protein Modeling Suite Can Do for You
journal, April 2010

  • Kaufmann, Kristian W.; Lemmon, Gordon H.; DeLuca, Samuel L.
  • Biochemistry, Vol. 49, Issue 14
  • DOI: 10.1021/bi902153g

Pfam: the protein families database
journal, November 2013

  • Finn, Robert D.; Bateman, Alex; Clements, Jody
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1223

Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding.
journal, October 1987

  • Matthews, B. W.; Nicholson, H.; Becktel, W. J.
  • Proceedings of the National Academy of Sciences, Vol. 84, Issue 19, p. 6663-6667
  • DOI: 10.1073/pnas.84.19.6663

Stabilization of hen egg white lysozyme by a cavity-filling mutation
journal, February 2001

Interface Matters: The Stiffness Route to Stability of a Thermophilic Tetrameric Malate Dehydrogenase
journal, December 2014

Protein thermal stability, hydrogen bonds, and ion pairs
journal, June 1997

  • Vogt, Gerhard; Woell, Stefanie; Argos, Patrick
  • Journal of Molecular Biology, Vol. 269, Issue 4
  • DOI: 10.1006/jmbi.1997.1042

Structural, Biochemical, and Computational Characterization of the Glycoside Hydrolase Family 7 Cellobiohydrolase of the Tree-killing Fungus Heterobasidion irregulare
journal, January 2013

  • Momeni, Majid Haddad; Payne, Christina M.; Hansson, Henrik
  • Journal of Biological Chemistry, Vol. 288, Issue 8
  • DOI: 10.1074/jbc.M112.440891

Cell proliferation at 122 degrees C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation.
journal, August 2008

  • Takai, Ken; Nakamura, Kentaro; Toki, Tomohiro
  • Proceedings of the National Academies of Science , Vol. 105, Issue 31, p. 10949-10954
  • DOI: 10.3410/f.1132832.589917

Hydrophobic environment is a key factor for the stability of thermophilic proteins
journal, January 2013

  • Gromiha, M. Michael; Pathak, Manish C.; Saraboji, Kadhirvel
  • Proteins: Structure, Function, and Bioinformatics, Vol. 81, Issue 4
  • DOI: 10.1002/prot.24232

Protein thermal stability, hydrogen bonds, and ion pairs
journal, June 1997

  • Vogt, Gerhard; Woell, Stefanie; Argos, Patrick
  • Journal of Molecular Biology, Vol. 269, Issue 4
  • DOI: 10.1006/jmbi.1997.1042

Electrostatic contributions to the stability of hyperthermophilic proteins 1 1Edited by J. M. Thornton
journal, June 1999

Increasing the thermostability of staphylococcal nuclease: implications for the origin of protein thermostability
journal, October 2000

  • Chen, Junmei; Lu, Zhiqiang; Sakon, Joshua
  • Journal of Molecular Biology, Vol. 303, Issue 2
  • DOI: 10.1006/jmbi.2000.4140

Polysaccharide hydrolase folds diversity of structure and convergence of function
journal, March 1997

  • Himmel, Michael E.; Karplus, P. Andrew; Sakon, Joshua
  • Applied Biochemistry and Biotechnology, Vol. 63-65, Issue 1
  • DOI: 10.1007/bf02920433

Coevolutionary Patterns in Cytochrome c Oxidase Subunit I Depend on Structural and Functional Context
journal, October 2007

The upper limits of enzyme thermal stability
journal, July 1996

Effective factors in thermostability of thermophilic proteins
journal, February 2006

Methionine Aminopeptidases from Mycobacterium tuberculosis as Novel Antimycobacterial Targets
journal, January 2010

Contribution of Electrostatic Interactions, Compactness and Quaternary Structure to Protein Thermostability: Lessons from Structural Genomics of Thermotoga maritima
journal, February 2006

  • Robinson-Rechavi, Marc; Alibés, Andreu; Godzik, Adam
  • Journal of Molecular Biology, Vol. 356, Issue 2
  • DOI: 10.1016/j.jmb.2005.11.065

Hydrophobic Effect on the Stability and Folding of a Hyperthermophilic Protein
journal, April 2008

  • Dong, Hongju; Mukaiyama, Atsushi; Tadokoro, Takashi
  • Journal of Molecular Biology, Vol. 378, Issue 1
  • DOI: 10.1016/j.jmb.2008.02.039

Kinetics and Thermodynamics of Ligand Binding to a Molten Globular Enzyme and Its Native Counterpart
journal, October 2008

  • Vamvaca, Katherina; Jelesarov, Ilian; Hilvert, Donald
  • Journal of Molecular Biology, Vol. 382, Issue 4
  • DOI: 10.1016/j.jmb.2008.07.049

Energetics of protein-protein interactions: Analysis ofthe Barnase-Barstar interface by single mutations and double mutant cycles
journal, January 1995

Additivity of mutational effects in proteins
journal, September 1990

Conservation of rapid two-state folding in mesophilic, thermophilic and hyperthermophilic cold shock proteins
journal, March 1998

  • Perl, Dieter; Welker, Christine; Schindler, Thomas
  • Nature Structural Biology, Vol. 5, Issue 3
  • DOI: 10.1038/nsb0398-229

Automated selection of stabilizing mutations in designed and natural proteins
journal, January 2012

  • Borgo, B.; Havranek, J. J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 5
  • DOI: 10.1073/pnas.1115172109

Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding.
journal, October 1987

  • Matthews, B. W.; Nicholson, H.; Becktel, W. J.
  • Proceedings of the National Academy of Sciences, Vol. 84, Issue 19, p. 6663-6667
  • DOI: 10.1073/pnas.84.19.6663

Native protein sequences are close to optimal for their structures
journal, September 2000

  • Kuhlman, B.; Baker, D.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 19
  • DOI: 10.1073/pnas.97.19.10383

Flexible structure alignment by chaining aligned fragment pairs allowing twists
journal, September 2003

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009

  • Cantarel, B. L.; Coutinho, P. M.; Rancurel, C.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn663

Proteins from thermophilic and mesophilic organisms essentially do not differ in packing
journal, October 1998

Protein sequence entropy is closely related to packing density and hydrophobicity
journal, February 2005

  • Liao, H.; Yeh, W.; Chiang, D.
  • Protein Engineering, Design and Selection, Vol. 18, Issue 2
  • DOI: 10.1093/protein/gzi009

Protein structure and evolutionary history determine sequence space topology
journal, February 2005

Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
journal, February 2007

  • Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
  • Science, Vol. 315, Issue 5813, p. 804-807
  • DOI: 10.1126/science.1137016

High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis
journal, June 1989

Cooperative Effect of Two Surface Amino Acid Mutations (Q252L and E170K) in Glucose Dehydrogenase from Bacillus megaterium IWG3 on Stabilization of Its Oligomeric State
journal, June 2005

Denatured States of Proteins
journal, June 1991

Mechanisms for stabilisation and the maintenance of solubility in proteins from thermophiles
journal, January 2007

Interface Matters: The Stiffness Route to Stability of a Thermophilic Tetrameric Malate Dehydrogenase
journal, December 2014

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